# Life in the frozen Ocean

Marcel Babin, Jody W Deming, Eric Maréchal, Josephine Z Rapp, Søren

Rysgaard, Martin Vancoppenolle

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## To cite this version:

Marcel Babin, Jody W Deming, Eric Maréchal, Josephine Z Rapp, Søren Rysgaard, et al., Life in the frozen Ocean. Annual Review of Marine Science, 2025, 10.1146/annurev-marine-032123-025316. [https://hal.science/hal-05368545](https://hal.science/hal-05368545)

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ANNUAL
REVIEWS

*Annual Review of Marine Science*

# Life in the Frozen Ocean

Marcel Babin,<fnref n="1" /> Jody W. Deming,<fnref n="2" /> Eric Maréchal,<fnref n="3" /> Josephine Z. Rapp,<fnref n="4" /> Søren Rysgaard,<fnref n="5" /> and Martin Vancoppenolle<fnref n="6" />

Annu. Rev. Mar. Sci. 2026. 18:7.1–7.25

The *Annual Review of Marine Science* is online at marine.annualreviews.org

https://doi.org/10.1146/annurev-marine-032123-025316

Copyright © 2026 by the author(s).
All rights reserved

## Keywords

sea ice, microbe, polar, adaptation, evolution, cold

## Abstract

Present seasonally or year-round in polar and subpolar seas, sea ice is one of the most complex and biologically rich ecosystems on Earth. Throughout the history of our planet, sea ice has periodically covered vast proportions of the world's oceans, and it may also serve as a plausible habitat on other ocean worlds. In this review, we provide a comprehensive overview of current knowledge on sea ice as a habitat, both on Earth and in extraterrestrial environments. We focus on bacteria, microalgae, and their associated viruses, describing the key physicochemical characteristics that shape this unique ecosystem. Additionally, we explore hypotheses on how microorganisms colonize sea ice, survive by protecting themselves and altering their environment, and ultimately proliferate and evolve. Finally, we consider the potential role of the sea-ice microbiome in the evolution of life on Earth and its possible existence beyond our planet.

<figure><img src="image_4.png" /></figure>

<footnote n="1">¹Takuvik International Research Laboratory, IRL 3376, CNRS and Université Laval, Québec City, Québec, Canada; email: marcel.babin@takuvik.ulaval.ca</footnote>

<footnote n="2">²School of Oceanography and Astrobiology Program, University of Washington, Seattle, Washington, USA; email: jdeming@uw.edu</footnote>

<footnote n="3">³Laboratoire de Physiologie Cellulaire et Végétale, UMR 5168, CNRS, CEA, INRAE, and Université Grenoble Alpes, Grenoble, France; email: eric.marechal@cea.fr</footnote>

<footnote n="4">⁴REV Ocean, Lysaker, Norway; email: josephine.rapp@revocean.org</footnote>

<footnote n="5">⁵Center for Ice-Free Arctic Research, Department of Biology, Aarhus University, Aarhus, Denmark; email: rysgaard@bio.au.dk</footnote>

<footnote n="6">⁶Laboratoire d'Océanographie et du Climat, CNRS, IRD, MNHN, and Sorbonne Université, Paris, France; email: martin.vancoppenolle@locean.ipsl.fr</footnote>
# INTRODUCTION

**Sea ice:** ice that forms from seawater and floats on the ocean

Abiotic interfaces within the biosphere are intense sites of chemical and physical processes with exchanges of heat, momentum, and matter. The extreme gradients that characterize them almost always create favorable environments that concentrate vital resources, and they frequently become hotspots for living organisms, particularly microbes. Interfaces are often abrupt, marked by dramatic phase transitions—solid-liquid, solid-gas, or liquid-gas—or sometimes softer transitions (e.g., the pycnocline in the upper ocean). Interfaces also create a conducive environment for interactions between individuals of the same or distant taxa, such as reproduction and parasitism. This is especially true when the fractal dimension of an interface is high, fostering the development of dense communities (Schmid 1999).

In polar and subpolar seas, sea ice—a three-dimensional porous interface with a high microscopic fractal dimension—is seasonally or permanently present as a boundary between the atmosphere and the ocean. Sea ice could actually be the richest and most multifaceted interface ecosystem on Earth (Arrigo 2014). Sometimes present over a large part of the global ocean throughout the history of our planet, it could also serve as a plausible habitat on other ocean worlds.

In this review, we provide a state-of-the-art overview of what we know about sea ice as a habitat, both on Earth and potentially on other suitable planets. We put most emphasis on microbes: bacteria, archaea, protists (including microalgae), and their viruses. After a few generalities and a brief review of microorganisms observed in sea ice, we explore how the process of sea-ice formation actually transforms the ice into a hospitable habitat. We then describe the key physicochemical characteristics of this ecosystem. We discuss current hypotheses explaining how microorganisms colonize sea ice, survive by protecting themselves and manipulating their environment, and subsequently proliferate and evolve. Finally, we discuss the potential role that the sea-ice microbiome may have played in the evolution of life on our planet and its possible existence on other planets.

# SEA ICE: WHERE AND WHEN

Sea ice is essentially present in the Arctic, sub-Arctic, and Southern Ocean waters. The Arctic sea-ice extent varies from 6.5 million km² around the fall equinox to 15.5 million km² around the spring equinox, and the Antarctic extent varies from 2.5 to 18.5 million km² (Serreze & Meier 2019). The difference between the two seasonal extremes corresponds to the so-called seasonal ice zone, where first-year ice (FYI) melts and re-forms each year. The annual minimum corresponds to the area with multiyear ice (MYI), which survives at least one melting season and can last for several years in the Arctic.

While the southern limit of Antarctic sea ice is constrained by the continent and ice shelves (maximum ~78°S) and its northern limit is constrained largely by the polar front (around 60°S), the northern boundary of Arctic sea ice is the North Pole, with its southern limit around the spring equinox ranging from approximately 80°N (Svalbard) to 44°N (Hokkaido and St. Lawrence River), depending on the longitude. These large differences between the two hemispheres result in Arctic sea-ice organisms experiencing much more variable light regimes along seasons and latitudes, with the regions farthest north going through long periods of deep polar night and midnight sun.

Today, the average thickness of sea ice is approximately 2 m in the Arctic and approximately 1 m in Antarctica. MYI that builds up against the northern coast of Canada and Greenland can be significantly thicker and can reach several tens of meters in pressure ridges commonly found in polar ice packs.

Sea ice is generally covered with snow in winter. The snow cover, which acts as an effective insulator that hinders the loss of heat from the ocean to the atmosphere and thus the growth of sea

<figure><img src="image_5.png" /></figure>
ice, reaches approximately 30 cm in thickness in the Arctic and almost double that in Antarctica. In the latter case, sea ice can display a negative freeboard because of the weight of the snow, often resulting in the flooding of the snow base by seawater and brine and the conversion of snow into ice.

## THE SEA-ICE BIOTOPE AT MULTIPLE SCALES

The most telling sign of life within sea ice is its green or brown coloration, often observed in the last few centimeters at the base of ice floes, especially in spring and sometimes at other heights depending on the type of ice (FYI or MYI). This coloration simply reveals the presence of a large number of pigmented microalgae.

Sea ice offers a unique habitat that is far more prone to microbial life than freshwater ice due to its porous nature, akin to a sponge, and the presence of liquid water (brine) within its structure despite temperatures often lower than -10°C. The presence of micrometer-to-millimeter liquid inclusions in sea ice arises from the saline character of seawater from which sea ice forms. The crystalline lattice of solid H₂O is not prone to the inclusion of external elements (Weeks & Ackley 1986). Consequently, sea salts and gases remain dissolved in the liquid phase. Although most of the liquid and the associated material is rapidly expelled from the ice as it forms, a small fraction remains trapped. This process leads to a complex matrix, consisting of dominant pure ice crystals and liquid inclusions with concentrated dissolved sea salts and gases, hydrated minerals, and gas bubbles (Hunke et al. 2011, Light et al. 2003).

It is within the brine inclusions that microorganisms can thrive. These inclusions first appear as thin layers less than 1 mm thick, giving sea ice the appearance of a mille-feuille with layers oriented vertically. Inclusions rapidly organize into a network of channels of different shapes and sizes reaching up to several millimeters in diameter (Middleton et al. 2022) that allow for convective motion.

Thermodynamic equilibrium constraints impose large variations in brine volume and composition. Brine inclusions maintain their freezing temperatures according to their salinity, which the ambient temperature adjusts by shrinking or expanding the size of the inclusion. As a result, the brine volume fraction in sea ice increases with the temperature and bulk salinity (i.e., the absolute salinity of a well-stirred melted sea-ice sample, which is much larger than the largest individual brine inclusions) of the sea ice, ranging from 0% at less than -36.2°C to a few percent at -20°C to greater than 20% for near-freezing temperatures (-1.9°C for seawater). Meanwhile, the salinity of brine inclusions ranges from 250 g/kg (seven times more than the salinity of typical seawater, 34 g/kg) at -36.2°C to much less than 30 g/kg near 0°C.

During the ice growth season, the bare ice surface, in contact with the atmosphere, is relatively cold (say, -20°C), whereas the ice base is warmer, being near the seawater freezing point. Between its surface and base, the sea-ice temperature increases downward quasi-linearly. In the presence of snow, the vertical temperature profile differs due to the insulating properties of the snow. Temperature drops more rapidly in the snow and more gently in the sea ice. In response to this temperature gradient, heat diffuses upward by conduction, leading to a heat deficit at the ice base, forcing the congelation (growth) of new ice at the ice-ocean interface. In FYI, the vertical profile of bulk salinity in winter typically has a C shape, with minimum values of approximately 5 g/kg at intermediate depths. Mostly due to the effect of warming temperature, the brine volume fraction increases downward, reaching its largest values near the ice base. Permeability, which determines the connectivity of the brine inclusion network, increases dramatically at a 5% brine volume fraction (Golden et al. 1998). Hence, in practice a relatively thin (5-20 cm) layer right above the ice base is prone to natural and forced convection with the underlying ocean (Rees Jones & Worster 2013), allowing for fluid and nutrient exchanges with the ocean (Vancoppenolle et al. 2010) that are critical to life within that layer.

**Freeboard:** the
distance from the
water line to the top of
sea ice

**Brine:** a solution of
high concentration of
salt in water, in this
context formed from
seawater during the
congelation (growth)
of sea ice

**Ice floe:** a large pack
of floating sea ice,
ranging from tens of
meters to many
kilometers in size

<figure><img src="image_6.png" /></figure>
**Sympagic:** living within ice

During the melting process that begins in spring at lower latitudes and continues until September in the Arctic and February in the Antarctic at high latitudes, the sympagic (within ice) ecosystem undergoes profound modifications. The first sign of change is a temperature increase in the ice that is due mainly to the return of solar light. In response, porosity increases, and the connectivity of the inclusion network grows. In the Arctic, the ice melts from the surface, which generates meltwater above the seawater line. Under the pressure head, meltwater percolates through the brine network, pushing a significant portion of brine and everything it contains, including microorganisms, into the ocean. Percolating meltwater also implies a near-surface desalination. In both hemispheres, ice also melts from the base; if this melting happens too rapidly, it can cause an abrupt halt in the production of microalgae in that bottom ice layer.

The thermochemical processes described above that accompany the growth and melting of sea ice largely determine the vertical variations in the microphysical and chemical properties of the ice pack. These properties shape the microhabitats in which sympagic microorganisms reside. Additionally, the flooding of sea ice by seawater and brine when the freeboard is negative under the weight of snow may significantly alter these properties at the top and eventually lead to a top-down colonization by microorganisms. This flooding process is prevalent mostly in the Antarctic. MYI also exhibits distinct characteristics because it has undergone one or more cycles of growth and partial melting. It is thicker and, in the Arctic, less saline than FYI. Observations may reveal several layers where microorganisms develop and concentrate, likely originating from each successive season of growth. On a larger scale, the drift and deformation of the ice pack come into play as winds and currents move the ice around, creating thick pressure ridges where ice floes converge and forming wide openings or leads where there is divergence, exposing the surface ocean to the atmosphere.

## LIVING CONDITIONS WITHIN THE BRINE INCLUSIONS

Brine inclusions constitute unique microenvironments that support life under extreme conditions. Depending on temperature, these inclusions can be generously wide for microbes, measuring millimeters thick and centimeters long (channels in warm bottom sea ice) or narrow to the point of preventing microbial movement and limiting chemical exchange (veins in upper winter sea ice; Krembs et al. 2011, Perovich & Gow 1996). As temperatures drop below -20°C, brine inclusions shrink to veins of nanometer-scale thickness, restricting microbes to triple-point junctures between ice crystals where the inhabitable space still measures in micrometers (Junge et al. 2004). Despite these spatial extremes and harsh fluctuations in temperature, salinity, gas composition, pH level, nutrient availability, and organic matter (Figure 1), organisms survive and thrive in sea ice. Understanding the dynamics of these conditions sheds light on the resilience and adaptability of life in extreme environments. Brine inclusions provide adequate space for not only microorganisms (throughout the ice) and algae (usually at warmer ice temperatures) but also small invertebrates that prey on sympagic residents. The temperature-dependent spatial constraints thus influence the population density and community structure of organisms residing within these microenvironments.

Psychrophilic (cold-adapted) organisms have evolved mechanisms to thrive in sea ice, exhibiting growth down to -15°C and metabolic activity at even lower temperatures (Ewert et al. 2025, Junge et al. 2004). Lower temperatures lead to higher salt concentrations in the brine inclusions. Halophiles—organisms adapted to high-salinity conditions—dominate brine inclusion communities, utilizing specialized mechanisms to maintain osmotic balance and enzymatic activity (Ewert & Deming 2013).

Brine inclusions contain a diverse array of dissolved gases (Crabeck et al. 2014, Tison et al. 2017). Gas composition fluctuates due to biological processes, environmental interactions, and

<figure><img src="image_7.png" /></figure>
<figure><img src="image_8.png" /><figcaption>Figure 1</figcaption></figure>

Seasonal influence of environmental conditions in sea-ice microhabitats on microbial communities. In autumn and winter, sea ice forms and thickens, reaching its maximum thickness in spring. Snow accumulation often increases throughout spring, and as summer approaches, melting snow and ice can create melt ponds that cover the sea-ice surface.

exchanges with air, ice, and water. Gases play crucial roles in metabolic processes for organisms inhabiting brine inclusions. Microorganisms in sea ice consume oxygen while respiring under aerobic conditions. As populations grow and consume oxygen, anaerobic conditions may develop in localized areas within the ice-brine system (Rysgaard et al. 2008). This depletion may facilitate anaerobic processes such as denitrification and anammox (Rysgaard & Glud 2004), likely impacting the availability of inorganic nitrogen within the ice.

Vertical pH profiles from melted ice-core sections reveal a consistent C shape during columnar ice growth, with the highest pH values (>9) both in exterior (top and bottom) ice sections and in frost flowers (formations on the surface of bare ice) and the lowest (~7) in interior ice sections (Hare et al. 2013). The pH levels within brine inclusions vary depending on microbial activity, chemical reactions, and environmental influences. Organisms within these microenvironments demonstrate remarkable adaptability to pH fluctuations, utilizing various biochemical mechanisms to regulate internal pH and maintain cellular homeostasis (McMinn 2017).

Brine inclusions also contain a complex mixture of inorganic nutrients (e.g., nitrate, silicate, and phosphate) and organic matter (from amino acids to large complex polysaccharides) derived from the surrounding seawater, atmospheric deposition, and in situ biological activity (Krembs et al. 2002). These substances serve as essential resources for microbial metabolism, growth,

**Columnar ice:** sea ice made up of flat, vertically elongated crystals that can reach several centimeters in diameter and tens of centimeters in length

<figure><img src="image_9.png" /></figure>
**Frazil ice:** small (a few to tens of millimeters long) ice crystals suspended in seawater that form during the first stages of sea-ice growth

**Granular ice:** sea ice with a granular texture that is generally found in the upper layer of sea ice and often forms from consolidated or frozen frazil ice

and reproduction within brine inclusions. Microorganisms exhibit diverse metabolic strategies to utilize available nutrients and organic matter, contributing to nutrient cycling and ecosystem functioning within these confined spaces (Rapp et al. 2021).

Living conditions within brine inclusions represent a remarkable example of life thriving in extreme environments. Despite the challenges posed by limited space, fluctuating temperature and salinity, variable gas composition, and shifts in pH and resource availability, sympagic organisms exhibit exceptional adaptability and resilience. Understanding these dynamics provides insights into the diversity, ecology, and evolution of life in extreme environments and informs our broader understanding of habitability beyond Earth (Martin & McMinn 2018).

## THE SEA-ICE BIOCENOSIS

The porous nature of sea ice, with its vast network of liquid microhabitats, serves as a refuge where microbes are sheltered from grazers and predators larger than a few millimeters, and even from smaller predators within the confines of the interior brine network. Among the microorganisms are numerous representatives of bacteria and archaea (Staley & Gosink 1999), fungi (Hassett et al. 2019), and protists, including microalgae and protozoa. Bacteria dominate over archaea by a large margin (>90%), with aerobic and facultatively anaerobic heterotrophs in the gammaproteobacterial, flavobacterial, and alphaproteobacterial orders almost always present; ammonia-oxidizing archaea are of increasing interest, as they may contribute nitrate in support of photoautotrophs (Firth et al. 2016). Microalgae are dominated by diatoms (especially pennate diatoms) and dinoflagellates but also include various other flagellates (haptophytes, chrysophytes, prasinophytes, and cryptophytes) (Poulin et al. 2011). Protozoa are dominated by ciliates but also include gymnamoebae, foraminifera, acantharians, and radiolarians (Caron et al. 2017). Viruses represent the lower end of the size spectrum (Yau & Seth-Pasricha 2019), and small animals (metazoans) represent the higher end. Double-stranded DNA viruses that infect bacteria can be found in high concentrations, while the larger and less well-studied eukaryotic RNA viruses represent less than 10% of the viral population (Rapp et al. 2025). Crustaceans within the warmer channelized portion of sea ice are dominated by copepods (Arndt & Swadling 2006), and crustacean larvae (nauplii), as well as nematodes, rotifers, polychaetes, flatworms, and hydrozoans, are also present (Bluhm et al. 2018).

## SEA-ICE COLONIZATION AND DECOLONIZATION PROCESSES

Sea ice has long been known to harbor numerous living organisms within, above, and/or at its base, notably microscopic ones (Garrison et al. 1989, Spindler 1994). Since at least the 1980s, there has been speculation about how microorganisms colonize sea ice. An enrichment of newly forming sea ice with microbes—by a factor of up to 20,000 compared with seawater—has been observed (Gradinger & Ikävalko 1998). This enrichment cannot be explained in terms of growth within the sea ice (Garrison et al. 1983). The most commonly proposed hypothesis for the mechanism of sea-ice colonization is so-called scavenging (Figure 2). During the initial growth phase of sea ice in the autumn, under the usual turbulent conditions at the sea surface, frazil ice (millimeter-sized ice crystals suspended in seawater) generally forms and rises to accumulate at the surface. When turbulence ceases, due to either calming weather or the stabilizing effect of frazil ice accumulating into an increasingly thick layer, a consolidated granular ice cover several centimeters thick eventually forms at the surface. Columnar ice then begins to grow, reaching a thickness of several tens of centimeters. As long as the initial frazil ice remains fluid or unconsolidated, the action of waves can produce vertical movements of the ice by stirring or pumping. Suspended particles, including microbes, may then be captured by the moving frazil grains, which

<figure><img src="image_10.png" /></figure>
a Scavenging

<figure><img src="image_11.png" /></figure>

b Nucleation

<figure><img src="image_12.png" /></figure>

c Motility

<figure><img src="image_13.png" /></figure>

d Buoyancy

<figure><img src="image_14.png" /></figure>

e Infiltration

<figure><img src="image_15.png" /></figure>

f Deposition

<figure><img src="image_16.png" /><figcaption>Figure 2</figcaption></figure>

Schematics of six different sea-ice colonization processes for microalgae (green): (a) scavenging, (b) nucleation, (c) motility, (d) buoyancy control, (e) infiltration, and (f) atmospheric deposition.

have a high surface-to-volume ratio. This phenomenon would contribute to the concentration of particles at the sea surface within sea ice. It may be particularly relevant in the convergence zone of Langmuir cells (Garrison et al. 1989). Why and how microbes associate with frazil grains remain mysterious. Is there an active microbial adherence mechanism? For example, some marine bacteria produce adhesins [a form of ice-binding protein (IBP)] that enable their adherence to ice, which, in turn, may enable diatoms colonized by such bacteria to adhere to ice (Guo et al. 2017).

Ice nucleation, whether fortuitously or intentionally, is another mechanism sometimes put forward for the colonization of sea ice by microbes. The homogeneous freezing of pure water devoid of particles occurs around -39°C. Heterogeneous freezing of water in the presence of particles acting as ice-nucleating agents occurs at 0°C for freshwater and around -1.9°C for typical seawater. Supercooled water, which is liquid water at a temperature below the heterogeneous freezing temperature, is susceptible to having its freezing triggered by the presence of ice-nucleating particles that promote water crystallization. This phenomenon has been extensively studied in the atmosphere due to the significance of aerosols as ice-nucleating particles in clouds, where supercooled water droplets freeze more easily in their presence. Clouds containing ice crystals have a lower albedo than liquid clouds, which has implications for climate (Murray et al. 2021). Among the aerosols that can act as ice-nucleating particles are dust, sea salts, pollen, fungi, and microbes (Huang et al. 2021), including microalgae such as diatoms (Eickhoff et al. 2023). Seawater contains a high abundance of both bacteria and microalgae and their debris, some of which have demonstrated ice-nucleating abilities once aerosolized. The presence of supercooled water at the

<figure><img src="image_17.png" /></figure>
ocean's ice-water interface suggests that ice nucleation could occur there, leading microbes, once surrounded by ice crystals, to rise and accumulate in sea ice. Although often mentioned in the literature, microbial ice nucleation has not been demonstrated in seawater, only freshwater. Bacteria with ice-nucleating proteins, present as epiphytes on lake diatoms, led to the accumulation of both ice and microbes at a lake surface (D'Souza et al. 2013).

Several species of microalgae are capable of motility, notably dinoflagellates with one or more flagella. Diatoms are devoid of flagella, except in the male gametes of centric diatoms. Only penate diatoms equipped with a raphe are capable of motility on a solid substrate, allowing, for example, microphytobenthic species to perform vertical migrations to regulate access to light at the surface and nutrients at depth according to tidal and solar cycles (Barnett et al. 2020). Pennate diatoms, such as those of the genus *Navicula*, are highly abundant within sympagic microalgae communities. Some sea-ice diatoms are capable of vertical migrations within the ice matrix (Aumack et al. 2014, Zhang et al. 2024), as are dinoflagellates like *Polarella glacialis*. Although the motility of microalgae within sea ice has been documented, we can only speculate on what role this ability could play in colonizing or entering sea ice. As for heterotrophic marine bacteria, many are well-known for motility, even under the more extreme conditions inside sea ice. The model sea-ice bacterium *Colwellia psychrerythraea* strain 34H can swim at -10°C in a solution kept liquid by organic solutes and sea salts (Junge et al. 2003). It also demonstrates chemotaxis (directed movement toward an organic compound), halotaxis (directed movement toward salt), and chemohalotaxis (directed movement toward both) at -8°C, suggesting an ability to both colonize sea ice and move within the interior brine network to optimize its position (Showalter & Deming 2018).

The control of buoyancy is another ability that may allow both microalgae and bacteria to migrate vertically in the water column. Present in several microalgal taxonomic groups, notably diatoms and dinoflagellates, buoyancy change is achieved through gas vacuoles, modification of the composition of intracellular organic matter (particularly lipids), or adjustments to the internal quantity of heavy ions (Arrieta et al. 2020, Lavoie et al. 2015). Several dominant bacterial taxa in sea ice, including members of the Alpha- and Gammaproteobacteria as well as Bacteroidota, are also gas-vacuolated (reviewed in Rapp et al. 2025). Although rarely emphasized, buoyancy could also serve as a mechanism facilitating the microbial colonization and infiltration of sea ice.

Undeformed FYI following a typical thermodynamic growth sequence as described above represents only one of the different types of habitats colonized by sympagic microbes. The microphysical properties of FYI can vary further depending on the temperature and salinity of the source seawater, as well as the prevailing meteorological conditions during its formation. Other habitats include pressure ridges (Fernandez-Mendez et al. 2018); leads (Assmy et al. 2017); MYI (Lange et al. 2017); melt ponds (Hancke et al. 2022); the ice surface, in the case of flooding by negative freeboard (Fernandez-Mendez et al. 2018); frost flowers (Bowman & Deming 2010); platelet ice (Hoppmann et al. 2020); and the ice-ocean interface, where epiphytic communities develop (Poulin et al. 2014). The diversity of these habitats, including their formation processes and physicochemical properties, further complicates the issue of sea-ice colonization.

Discussion of colonization leads to the opposite phenomenon: decolonization of sea ice. Microbial movements between ice and the water column likely occur during all icy seasons; species capable of moving benefit from that ability, thriving or surviving in the different environments during some or all life stages. Numerous studies have documented multiple species of cosmopolitan microbes (i.e., from both sea ice and seawater; e.g., Rapp et al. 2025). It is even conceivable that all polar species of marine microbes can survive in one form or another in both ice and water, to the extent that the water column inoculates sea ice and vice versa. The latter is particularly evident in spring, when the ice drains much of its brine under the pressure of surface meltwater and the sea-ice base becomes ablated. These two events carry most of the microbiome into the water

<figure><img src="image_18.png" /></figure>
column. Some microbes are known to survive, thus inoculating the water column, while others will contribute to the export of carbon to ocean depths (Amiraux et al. 2017, 2020). Sea ice is also envisioned as a refuge for microbes, as well as a reservoir of inocula for the water column, further contributing to horizontal dissemination (Olsen et al. 2017). Over deep waters in particular, sea ice would play the same role of repository as sediments do in shallow areas.

# ADAPTATIONS TO EXTREME TEMPERATURE, SALINITY, AND LIGHT CONDITIONS

## Extracellular and Intracellular Adaptation Mechanisms

Microorganisms in sea ice must cope with highly variable temperatures, nutrient concentrations, salinity, and light. When combined, some parameters can mitigate the effect of others, like elevated salinity preventing the liquid environment from reaching the freezing point within the interior brine network. Taking photosynthetic microalgae as an example, the molecular mechanisms involved in the sensing of most of these environmental parameters are unknown (Figure 3, ①). The

<figure><img src="image_19.png" /><figcaption>Figure 3</figcaption></figure>

Schematic of possible molecular and cellular changes in a diatom during sea-ice colonization, highlighting the cell wall, plasma membrane, nucleus, mitochondria (limited by a two-membrane envelope), and plastid (limited by four membranes). Inside the plastid, suborganellar compartments include the photosynthetic membranes and a pyrenoid, where CO₂ is concentrated and captured. Some processes during ice colonization are uncharacterized. (①) The sensing mechanisms of environmental variations are unknown. (②) Signaling cascades and the activation/repression of nuclear transcription factors are unknown. (③) The production of EPS has been characterized. (④) The production of IBPs has been characterized. (⑤) Membrane glycerolipid remodeling processes are uncharacterized. Membranes where lipid composition is likely to be remodeled (i.e., the plasma membrane, mitochondria, plastid-limiting membranes, and thylakoids) are shown in red. (⑥) The accumulation of lipid droplets filled with triacylglycerol and carotenoids is uncharacterized. (⑦) The production and activation of specific plasma membrane transporters are unknown. (⑧) The specific biogenesis of plastoglobules filled with carotenoids (antioxidant compounds) and precursors of oxylipins is unknown.
Abbreviations: EPS, extracellular polymeric substances; IBP, ice-binding protein.

<figure><img src="image_20.png" /></figure>
signaling cascades that follow the sensing of abiotic changes from seawater to ice—possibly via receptors at the plasma membrane (Figure 3, ①)—and modulate genetic expression (Figure 3, ②) are also unknown. The scale of the genetic reprogramming and metabolic and physiological remodeling in a microbe during the colonization of sea ice also remains to be established.

Inside brine channels, the adaptation mechanisms are better known. They first involve specific responses, including biogenic production of microhabitat ice-active modifiers, such as extracellular polymeric substances (EPS) (Figure 3, ③) and IBPs (Figure 3, ④). Studies have suggested that EPS are involved in the entrapment, retention, and survival of microorganisms (Ewert & Deming 2013, Krembs et al. 2011, Mock & Thomas 2005). The EPS biosynthetic pathway was identified genomically in *Fragilariopsis cylindrus* (Aslam et al. 2018) and similarly revealed in the sea-ice bacterium *Psychroflexus torquis* (Feng et al. 2014). IBPs, which may also be embedded in EPS (Raymond 2011), have been characterized in a multitude of organisms (Bar Dolev et al. 2016). They participate in freeze avoidance (Kawahara et al. 2007), cryoprotection (Raymond et al. 2009), and ice adherence (Guo et al. 2017). IBPs are produced by some microalgae, including *Chaeto-ceros neogracile*, at freezing and deep-freezing temperatures (Bayer-Giraldi et al. 2020, Cho et al. 2019, Kim et al. 2017). Ice *Navicula* and *Pleurosigma* species can glide at temperatures as low as -15°C on the surface of ice substrates, a capability absent in temperate diatoms of the same genus (Zhang et al. 2024). This gliding ability highlights that, in addition to EPS and/or IBPs anchoring cells to sea ice, diatoms possess cytoskeleton polymers and motors that remain active at such low temperatures. EPS and IBPs may also contribute to structuring the ice habitat (Eickhoff et al. 2019, Krembs et al. 2011) and stabilizing the brine network during freezing (Krembs et al. 2002, Raymond et al. 2009). Several sympagic algae, including diatoms, prymnesiophytes, prasinophytes, and chlorophytes, and many sympagic bacteria secrete these substances, which are critical for their adaptation (Lyon & Mock 2014, Rapp et al. 2025).

In contrast to extracellular substances and proteins, less is known of intracellular processes ensuring cell integrity and the continuity of vital functions. General mechanisms involving membrane and storage glycerolipids operate in both prokaryotic and eukaryotic cells subjected to a decrease in temperature or to various nutrient stresses (Rapp et al. 2025). In algae, glycerolipids are usually involved in the protection of cellular and organellar integrity via a compositional remodeling, first by adjusting the relative proportions of phospholipids, galactolipids, and betaine lipids in membrane compartments (Figure 3, ⑤) and then by controlling the level of triacylglycerol in cytosolic lipid droplets (Figure 3, ⑥) (Abida et al. 2014, Ezzedine et al. 2023). Glycerolipid remodeling has recently been reported in an Arctic diatom in response to light spectral changes (Svenning et al. 2024), as well as in the snow alga *Sanguina nivaloides* (Ezzedine et al. 2023). If a remodeling of membrane lipids is also triggered in sea-ice microorganisms, it has not been established, whether at the onset of ice formation, following an increase in salinity, or following a depletion of some nutrients.

Microbes also need to keep maximal membrane fluidity to ensure the function of membrane-associated proteins (Renne & Ernst 2023). In microalgae, this fluidity is particularly important in photosynthetic membranes where photosystems are embedded. It is tunable in the various membrane glycerolipid classes by the control of fatty acid unsaturation and length, as reported for snow algae (Ezzedine et al. 2023). The tuning of fatty acids in some chlorophytes and in most stramenopiles further implies their conversion into very-long-chain polyunsaturated fatty acids, which were shown to correlate with cold in the first global ocean lipidome survey (Holm et al. 2022) and are well-known in psychrophilic bacteria, including *Colwellia psychrerythraea* and *Psychrobacter torquis* inhabiting sea ice (Rapp et al. 2025). The mechanisms controlling fatty acid length and saturation level in response to environmental factors have been little studied in Arctic and Antarctic algal species (Mock & Kroon 2002). Though still undemonstrated, a membrane glycerolipid

<figure><img src="image_21.png" /></figure>
remodeling can be expected to be triggered by ice formation, with activation of specific fatty acid desaturases and elongases that need to be characterized. In bacteria, genomics and proteomics are revealing strong potential for membrane remodeling in response to sea-ice conditions (Mudge et al. 2021, Rapp et al. 2021). A metabolic reallocation of carbon in the direction of triacylglycerol is also expected as an algal storage strategy for long-term survival at low temperature (Figure 3, ®).

Glycine betaine is a solute that enables many microbes to tolerate high salinity and freezing. Antarctic sea-ice diatoms express glycine betaine transporters at their cell surfaces, allowing them to scavenge this antifreeze solute (Torstensson et al. 2019). Plasma membrane transporters (Figure 3, ®) are therefore mobilized for ionic and solute exchanges, osmotic homeostasis, and nutrient import. Field experiments have demonstrated the use of solutes for halotolerance by whole microbial communities in sea-ice brines (Firth et al. 2016).

Eventually, high salinity and numerous abiotic stressors trigger an intracellular oxidative stress response in diatoms (Lupette et al. 2018). The production of radical oxygen species can be controlled by antioxidant compounds, including carotenoids accumulating in chloroplast plastoglobules (Figure 3, ®) or in cytosolic lipid droplets (Figure 3, ®), combined with triacylglycerol (Ezzedine et al. 2023). Oxidative stress can also trigger the enzymatic or nonenzymatic production of bioactive cyclopentane oxylipins, which act as signaling compounds (Lupette et al. 2018). In plants, the committing step of oxylipin biosynthesis is known to occur in plastoglobules (Figure 3, ®). None of these mechanisms have been characterized in Arctic or Antarctic microalgae. Among the dominant sea-ice bacteria, several produce membrane-bound carotenoid pigments, which have been implicated in oxidative stress response and protection against UV radiation, as well as regulation of membrane fluidity (Rapp et al. 2021). Just as principles guiding the colonization of sea ice are broadly similar between microalgae and bacteria, some similar protective molecular and intracellular responses of prokaryotic and eukaryotic cells have been characterized. The actual mechanisms involved in the maintenance of cell integrity and cell viability, however, remain elusive. The spatiotemporal choreography of these cellular processes needs to be addressed by multiomic approaches in relevant experimental designs and in appropriate model species (Figure 3).

## Survival of Photoautotrophs Under Dim Light Conditions

Sea ice at high latitudes is an environment where light conditions reach extremes, especially at the lower end of the natural range of variation. Indeed, sea ice and especially the snow covering it are highly scattering media that greatly attenuate solar radiation. Under typical 1.5-m-thick sea ice with a 20-cm layer of dry snow, the radiation reaching the base of the ice where ice microalgae most often develop is typically reduced by three orders of magnitude compared with the incident radiation (Oziel et al. 2019). In spring, as soon as the air temperature rises above 0°C, the snow cover rapidly melts, and melt ponds often appear on the ice. Under these conditions, 5-40% of the incident irradiance penetrates the sea ice (Perovich 2017) during daylight, which can sometimes extend for a full 24 hours. These conditions are conducive to phytoplankton blooms, but ice algae are generally already expelled from the ice by drainage or basal-layer ablation. Therefore, except for those that may eventually develop at the top of the ice following flooding, ice algae typically grow in low-light conditions, below 5 µmol photons m⁻² s⁻¹ at noon. Growth of ice microalgae has even been observed at less than 0.25 µmol photons m⁻² s⁻¹ in Greenland (Hancke et al. 2018). These observations raise several questions: What is the minimal irradiance allowing net growth in polar microalgae? Even when autotrophy does not allow for net growth, could it contribute to the survival of microalgae in very low light? And could it complement heterotrophy in microalgae capable of mixotrophy? Most microalgae, especially polar diatoms, are now known to survive for several months in darkness, even without resorting to heterotrophy (Joli et al. 2023, Sciandra et al. 2022). Raven et al. (2000) suggested that microalgae could theoretically grow at 0.01 µmol

<figure><img src="image_22.png" /></figure>
photons m⁻² s⁻¹. Observations have not confirmed this possibility in nature, because either the radiometers or the methods used to measure photosynthetic rates, such as radiolabeled-carbon fixation, were also not sensitive enough (Kvernvik et al. 2018). Recently, however, Hoppe et al. (2024) observed that the early-spring onset of chlorophyll *a* accumulation in the water column of the central Arctic Ocean began when the average daily photosynthetically active radiation reached a threshold of 0.04 µmol photons m⁻² s⁻¹.

At very low irradiance, photosynthesis could provide reducing power to the cell without necessarily involving carbon fixation or oxygen production. For example, cyclic electron flows in the photosynthetic apparatus can produce ATP directly usable by metabolism. Even in small quantities, such a mechanism could promote the survival of microalgae during the polar night until more favorable light conditions return in spring. Also, independently of carbon fixation, some heterotrophic bacteria in sea ice produce proteorhodopsins, generating enough energy from light to support growth under stressful sea-ice conditions (Feng et al. 2013).

Mixotrophy, the ability to utilize both photoautotrophy and chemoheterotrophy, emerges as an optimal nutritional mode for protists in polar sea-ice regions where the polar night can last for nearly six months. This mode is manifested primarily through phagotrophy but also occurs through osmotrophy when the cell wall prevents phagocytosis, as seen in diatoms (Meyer et al. 2022). In the Arctic, phagotrophy (mainly bacterivory) has been documented within phytoplankton for dinoflagellates, cryptophytes, chrysophytes, prasinophytes, and haptophytes, as well as in ciliates capable of acquired autotrophy (Stoecker & Lavrentyev 2018). In sea ice, observations confirming mixotrophy are rarer (Moorthi et al. 2009) and sometimes indirect (Søgaard et al. 2021). They are nonexistent for osmotrophy in protists. However, mixotrophy is certainly a highly important nutritional mode in polar seas, from both ecological and biogeochemical perspectives.

## Resistant Forms of Microorganisms

In ice algae, another strategy for surviving long periods of darkness or generally unfavorable conditions (e.g., low temperature, high salinity, or oligotrophy) is to develop resistant forms such as cysts and other dormant forms. The presence of cysts in sea ice has been documented for dinoflagellates and chrysophytes (Buck et al. 1992, Hegseth & von Quillfeldt 2022, Stoecker et al. 1997). Other taxonomic groups of microalgae and other microorganisms may also develop resistant or resting stages in sea ice, as has been widely documented within phytoplankton (Dzhembekova et al. 2018, McQuoid & Hobson 1996). Many bacteria in the colder sections of sea ice appear to undergo dormancy (Junge et al. 2004), channeling limited resources into maintenance energy until more growth-permissive conditions return.

## Epigenetic Memory

The initial entrainment into sea ice presents microorganisms with multiple stressors, from subzero temperature to hypersalinity and high concentrations of potentially infective viruses. To survive and become one of the canonical, environmentally selected sea-ice microorganisms, the means for rapid acclimation to the new, more extreme conditions must already be encoded genetically. Genomic studies have revealed genes involved in acclimation to freezing temperatures, such as those for cryoprotectant EPS (Feng et al. 2014, Methé et al. 2005) and ice-active compounds (Bayer-Giraldi et al. 2020, Carillo et al. 2015, Raymond et al. 2009), and to hypersalinity, such as those for accumulating compatible solutes or osmolytes (Firth et al. 2016, Torstensson et al. 2019), but obtaining a mechanistic understanding of the regulatory processes underlying their expression has been challenging. Important headway has been made through the study of epigenetics in diatoms, with the discoveries that a significant portion of their genomic

<figure><img src="image_23.png" /></figure>
DNA is methylated and that methylation patterns can be keyed to the regulation of specific genes (Tirichine et al. 2017, Veluchamy et al. 2013). The DNA of the model sea-ice diatom *Fragilariopsis cylindrus* (Mock et al. 2017) is significantly methylated and has an unprecedented density of clustered methylations (Tirichine et al. 2017), but experiments to link methylation patterns specifically to acclimation and successful habitation to sea ice are still needed.

In bacteria, DNA methylation represents a regulatory mechanism for rapid acclimation to stressors, as well as defense against viral infection. By methylating nucleotides in specific patterns, a bacterium can distinguish its own DNA from foreign DNA and use defensive enzymatic machinery to degrade incoming viral DNA. This epigenetic defense mechanism has been characterized as a form of memory, a means to respond rapidly to a new threat based on past experience (Riber & Hansen 2021). The recent acquisition of whole community metamethylomes has led to invoking DNA methylation as a regulatory mechanism to explain tolerance of changing conditions in the ocean, for example, within the distinctive age-specific strata of marine sediments (Rambo et al. 2019). This epigenetic mechanism has not been studied in sea ice even though entrainment into the ice and entrapment through the seasons provides an ideal natural experiment for investigating survival mechanisms against an onslaught of stressors. With the advent of relatively inexpensive DNA sequencing methodologies, progress in this area can be expected. Preliminary data from sea-ice brines indicate DNA methylation in patterns related to stress exposure time (Kanaan & Deming 2024). Although epigenetic for its role in rapid acclimation, DNA methylation that improves fitness is inheritable and thus could also help to explain the repeated success of some microbial taxa over others in the extreme environment of sea ice.

## SEA-ICE MICROBIOME DYNAMICS

The sea-ice microbiome refers to the diverse community of microorganisms inhabiting sea ice, including bacteria, archaea, algae, fungi, and viruses. These microorganisms play key roles in nutrient cycling through their diverse metabolic pathways and in the overall ecosystem dynamics within the ice and its surrounding environments.

### Nutrients

The nutrient content of sea ice is influenced initially by the nutrients present in the source seawater. Nutrient composition in the ice can thus vary depending on geographical location, season, and ice thickness (Meiners & Michel 2017). Nitrogen, an essential macronutrient for marine organisms, particularly in the forms of nitrate, nitrite, and ammonium, can be incorporated into sea ice from seawater during the freezing process. Ammonium may also be deposited from the atmosphere. Silicon is important for the growth of diatoms, as they utilize silicon to build their cell walls. Silicon concentrations in Arctic sea ice in coastal areas influenced by silicon-rich glacier melt can affect the distribution and abundance of diatoms following ice melt (Meire et al. 2016, 2023). The macronutrient phosphorus is required for cell metabolism and growth. Unlike nitrogen and silicon, phosphate is not considered a limiting nutrient for Arctic sea-ice algae or phytoplankton. In addition to macronutrients, the micronutrient iron is essential for algal growth. While iron concentrations in sea ice are not generally limiting, the potential colimiting role of other biologically required metals, including zinc, copper, and manganese, remains largely unstudied (Lannuzel et al. 2016).

### Metabolic Pathways and Growth

Microbes in sea ice utilize various metabolic pathways to survive and thrive, from photosynthesis and chemoautotrophy to heterotrophy and mixotrophy. Photosynthetic algae harness sunlight

<figure><img src="image_24.png" /></figure>
to produce organic carbon, while chemoautotrophic bacteria use chemical energy from inorganic compounds. Although sea-ice ecosystems are among the most extensive of Earth's habitats, their autotrophic and heterotrophic activities remain poorly constrained (Attard et al. 2018). Sea ice presents a challenge for productivity studies in that the ice pack is often an uneven surface with a patchy distribution of biotic communities (Glud et al. 2014, Katlein et al. 2015, Rysgaard et al. 2001). Traditionally, sea-ice algal productivity was measured using radiocarbon tracers, and heterotrophic activity was understudied. Recently, more studies (based on oxygen and eddy covariance techniques) have included both autotrophic and heterotrophic activities (Attard et al. 2018, Campbell et al. 2022), often finding that the system is net heterotrophic—that is, more oxygen is consumed by microbes than is produced by photosynthesizing algae. While oxygen is physically excluded from the ice phase into the gas and brine phases during freezing, later in summer the underlying water and meltwater from sea ice can be undersaturated and even anoxic within parts of the brine system (Rysgaard et al. 2008). This undersaturation potentially permits the use of anaerobic respiration pathways, such as denitrification and anammox, which in turn would reduce nutrient availability for primary producers (Rysgaard & Glud 2004). When oxygen levels are sufficient, however, nitrifying bacteria can regenerate nitrate for ice algae (Firth et al. 2016). Heterotrophic microbes in the ice rely on organic carbon sources for energy, initially entrained into the ice during freezing and later produced by autotrophs during spring, while mixotrophs switch between autotrophic and heterotrophic modes of nutrition depending on environmental conditions (Søgaard et al. 2021). The balance of microbial metabolic strategies in sea ice is influenced by multiple environmental factors, including temperature, salinity, nutrient availability, light penetration, and interactions with other organisms.

## Seasonal Variations

Seasonal variations significantly influence the dynamics of the sea-ice microbiome (Figure 1). During winter, low light and harsh conditions limit biological activity, leading to lower biomass and a reduced diversity of organisms within the ice and surrounding waters. The continuing growth of sea ice and accumulation of snow further restrict light penetration, inhibiting photosynthetic organisms (Campbell et al. 2017b, Lund-Hansen et al. 2020), while the overall habitat (brine volume) for the microbiome shrinks as temperatures drop.

At the same time, the formation of sea ice causes a rejection of salts, solutes, and gases into the brine phase, thus influencing the osmotic, nutrient, and gas contents of the brine within the ice (Crabeck et al. 2016, Rysgaard et al. 2011). Increased concentrations of CO₂ and O₂ (Rysgaard et al. 2008) affect biogeochemical transformations, variations in pH levels (Hare et al. 2013), and gas pressure in the brine system (Crabeck et al. 2019).

As spring approaches and sea ice begins to melt, brine volume expands and light availability increases, triggering an ice-algal bloom. Initially, this bloom may be dominated by smaller cells and pennate diatoms with low productivity and net heterotrophy. Parts of the brine system can be low in oxygen due to heterotrophic activity, hence favoring anaerobic processes (Rysgaard & Glud 2004). Over time, sea ice transitions into a more biologically active phase characterized by higher productivity and net autotrophy, with larger cells and centric diatoms becoming dominant (Campbell et al. 2017b, 2018). At the same time, increasing temperature and melting ice increase brine volume and permeability, facilitating greater CO₂ and O₂ exchange with the atmosphere and water column below. This process reduces CO₂ concentrations inside the sea ice and in surface waters, while photosynthetic activity and calcium carbonates dissolving in the brine system increase the pH (Glud et al. 2014, Rysgaard et al. 2011).

In early summer, the bottom layer of sea ice becomes highly productive, marked by elevated concentrations of chlorophyll *a* and particulate organic carbon, indicative of active growth and

<figure><img src="image_25.png" /></figure>
biomass accumulation (Lund-Hansen et al. 2020). This period of activity is intense but can be short, as the ice begins to melt more rapidly. As late-summer open water, where FYI has fully melted, transitions into autumn, new sea ice restarts the annual cycle with a net heterotrophic sea-ice ecosystem.

## SEA-ICE BRINES AS A SPACE FOR MICROBIAL DIVERSIFICATION AND EVOLUTION

Even though sea ice forms from seawater, the challenges experienced by microorganisms in sea ice differ fundamentally from those in the water column, selecting for members of the community best adapted to the physical, chemical, and biological stresses imposed by the seasonally dynamic brine environment. The genomic variations and features that confer adaptation can be inherited vertically upon cell division (sexual or asexual reproduction) but also via horizontal gene transfer (HGT), the transfer of genetic material from one organism to another without cell division. The main mechanisms of HGT are transformation, referring to the uptake of free DNA from the environment; transduction, where viruses act as transfer agents; and conjugation, the transfer of genetic material, including plasmids, by direct organism-organism contact. In sea-ice brines, elevated cell-to-cell and cell-to-virus contact rates, as well as high concentrations of extracellular free DNA relative to underlying seawater, coincide with external stress factors, like rapid changes in temperature and salinity, high UV radiation, and the presence of reactive oxygen species. These factors are known from laboratory studies to promote the activation of gene-exchange mechanisms, such as natural competence, viral lysis and the extracellular release of DNA, and mobile genetic elements. Thus, sea-ice brines may favor the occurrence of HGT and genetic diversification (Figure 4), a hypothesis supported by insights from a growing number of genomic studies (Rapp et al. 2025).

The importance of HGT and genome plasticity for survivability in sea ice is well-illustrated by the detailed genomic studies of dominant sea-ice bacteria from both poles (Feng et al. 2014, Vollmers et al. 2013). The genome of *Psychroflexus torquis*, a psychrophilic member of both Arctic and Antarctic sea-ice microbiomes, shows a much higher occurrence of HGT than its close nonpsychrophilic relatives, with most of the unique genomic features relevant for cold and salt adaptation, including for EPS and polyunsaturated fatty acid synthesis centered on genomic islands that show clear signatures of HGT (Feng et al. 2014). Similarly, the genomes of *Octadecabacter arcticus* and *Octadecabacter antarcticus* from Arctic and Antarctic sea ice, respectively, show evidence of HGT for numerous features that confer adaptation to the sea-ice habitat, including the acquisition and storage of nutrients. For example, *Octadecabacter arcticus* encodes a gene cluster for the synthesis and degradation of cyanophycin, a storage compound for nitrogen most closely related to a cluster found in *Colwellia psychrerythraea* 34H, while *Octadecabacter antarcticus* encodes the genes for assimilatory nitrate and nitrite reduction pathways on a mobilizable genomic island (Vollmers et al. 2013). Further genome plasticity may be achieved by the unusually high density of mobile genetic elements and plasmids, which could enhance adaptability to changing environmental conditions (Vollmers et al. 2013). Interestingly, 20% of genes present in these genomes were not shared, highlighting mechanisms of adaptive evolution unique to Arctic or Antarctic sea-ice environments (Vollmers et al. 2013).

In sea ice, viruses, bacteria, unicellular algae, and larger organisms coexist and coevolve (Figure 4), as exemplified by genomic evidence of transduction and cross-domain HGT. Viruses in sea-ice brines encode fatty acid desaturases originating from bacterial host genomes within the Bacteroidota and Proteobacteria phyla (Zhong et al. 2020), suggesting bacterium-to-virus gene transfers. Fatty acid desaturases are key enzymes in the maintenance of membrane fluidity at low temperatures; thus, viruses encoding such auxiliary metabolic genes have the potential to alter host

<figure><img src="image_26.png" /></figure>
<figure><img src="image_27.png" /><figcaption>Figure 4</figcaption></figure>

Environmental setting and individual mechanisms that can foster microbial gene exchange in sea ice. The center panel illustrates that high numbers of microbial cells and viruses coexist inside brines (blue), where they are exposed to abiotic stressors, including rapid changes in temperature, salinity, and UV radiation (yellow triangles). The production and release of EPS (pink) retain and preserve cells and free DNA, allowing for extended interactions. The focus panels show (a) the introduction of foreign DNA into prokaryotic cells via viruses and the release of DNA through viral lysis; (b) the introduction of foreign DNA into eukaryotic cells via viruses; (c) cross-domain gene exchange via direct cell contact; (d) gene exchange via phagocytosis, either cross-domain (e.g., bacteria to algae) or interdomain (e.g., through uptake of algae by mixotrophic algae); (e) the release of DNA via cell death and uptake of free DNA by neighboring cells; and (f) the transfer of DNA, including plasmids, via direct cell contact or pili. Genomic insights and other data from sea ice support the relevance of these mechanisms in sea ice, but pinpointing their occurrence in sea-ice brine remains elusive.
Organisms and viruses are not drawn to scale, but the center panel would be approximately 100 × 100 µm at −5°C. Abbreviation: EPS, extracellular polymeric substances.

cell fitness during subsequent infections (Breitbart et al. 2018). Several examples of cross-domain HGT between bacteria and microbial eukaryotes have also been documented, including the transfer of IBPs from bacteria to important sea-ice diatoms (Bayer-Giraldi et al. 2010, Raymond & Kim 2012). Recent work has highlighted potential mechanisms of interalgal HGT of IBPs, potentially through phagotrophic uptake of microalgae by other mixotrophic algae (Dorrell et al. 2023). Interestingly, IBP sequences with high homology to both bacterial and diatom IBPs were also found in the genome of an Antarctic sea-ice copepod, suggesting HGT to higher trophic levels (Kiko 2010). Although the origin of the IBP in the copepod genome could not be reconstructed with certainty, results suggested that these antifreeze proteins were probably transferred horizontally several times (Kiko 2010).

<figure><img src="image_28.png" /></figure>
POSSIBLE ROLE OF THE SEA-ICE MICROBIOME DURING
PAST ICE AGES

Our planet has gone through several periods during which the ocean was covered in ice over a much larger area than today, or even entirely during so-called Snowball Earth events (Hoffman et al. 1998). There were six major ice ages, the oldest dating to 2.5 billion years ago and the most recent ending at the beginning of the Holocene (Earle 2019). One of the two most intense glaciation periods was the Cryogenian (717–635 Mya). The Sturtian (717–660 Mya) and Marinoan (639–635 Mya) glaciations of that era are believed to be two Snowball Earth events that occurred just before the Cambrian explosion. Life existed mostly in the ocean at that time. Based on paleoceanographic data, cyanobacteria survived these two events. Similarly, eukaryotic microalgae that appeared before the Sturtian or Marinoan survived the following glaciations (Brocks et al. 2017, Cohen & Kodner 2022). One might then wonder how these photoautotrophs could survive if the ocean was completely covered in ice. What type of ice was it?

Different scenarios have been put forward using models (Figure 5). Of general agreement is that, except possibly near the equator, the ocean was covered by a layer of ice several hundred

<figure><img src="image_29.png" /><figcaption>Figure 5</figcaption></figure>

Ice-covered oceans on Snowball Earth and an icy moon. (a) Three possible scenarios of latitudinal distribution and thickness of oceanic ice during Snowball Earth events (inspired by the material at https://www.snowballearth.org/slides.html). Glacier (meteoric) ice and sea ice are separately color-coded. (b) A simple representation of how the ice cover over an ocean may appear (thickness, temperature profile, fissures, and surface plumes) on a moon such as Enceladus.

<figure><img src="image_30.png" /></figure>
**Meteoric ice:** ice forming from precipitation water (snow and rain)

meters thick that some researchers have conceptualized as a marine glacier, consisting of meteoric ice in its upper part and sea ice in its lower part. Near the equator, the ocean could have been ice-free (Peltier et al. 2004) or covered with relatively thin sea ice (Pollard & Kasting 2005) or with a marine glacier thinner than those at high latitudes but still more than 100 m thick (Warren et al. 2002). In the first two scenarios, microalgae could have survived in the water column and/or in brine channels in sea ice. In the third scenario, photosynthesis was probably impossible at the base of the marine glacier, being too thick to transmit enough light. The lower light limit for photosynthesis, however, is still poorly understood. Additionally, what was the transmittance of light through this glacier if it was devoid of a snow cover and perhaps covered with melt ponds? Assuming that the marine glacier was indeed too thick to allow photosynthesis at its base, even at the equator, how could microalgae survive in this context? Inland seas such as the Red Sea may have been shielded from the invasion of the marine glacier, remaining ice-free or covered in sea ice (Campbell et al. 2014, 2017a). Microorganisms may have continued to thrive on the surface of the marine glacier, as can still be observed today in Antarctica and the Arctic (Hawes et al. 2018, Vincent & Howard-Williams 2000). Also, some tropical ocean areas may have remained ice-free (Song et al. 2023). We also wonder whether multiple large fractures throughout the thickness of the marine glacier resulting from its large-scale dynamics could have created large leads covered with sea ice, which could host a sympagic microbiome or allow a marine benthic or planktonic microbiome to develop.

It is intriguing that eukaryotic microalgae started dominating primary production after the first Cryogenian Snowball Earth event and the Ediacaran–Cambrian rise of macroscopic life followed the second. Numerous hypotheses have been proposed to explain this coincidence (e.g., van Maldegem et al. 2019). Not yet considered is whether the marine ice microbiome may have played a role, given the concentrating effect of sea-ice formation on microbes and the stressors of the habitat understood to promote genetic exchange (see above). Although studies have focused on the exchange of genes that would facilitate adaptation to the sea-ice habitat itself, other gene transfers may occur in the ice that are not selected until the receiving microbes have been released from the ice to flourish in a more clement environment. Sea ice could serve as a hotspot for gene exchange mechanisms, influencing adaptation and evolution in the less harsh ocean at large.

## POSSIBLE SEA-ICE MICROBIOME IN OTHER OCEAN WORLDS

Besides Earth, our solar system hosts five confirmed ocean worlds: the Jovian moons Europa, Callisto, and Ganymede and the Saturnian moons Enceladus and Titan (Hendrix et al. 2019), with more to be counted (Hall 2020). Unlike Earth's ocean today, these oceans are completely covered by thick crusts of ice, with thickness estimates ranging from 3 km to more than 30 km, though the actual distances from the surface to the ocean below are debated and may vary by location. Of the icy moons with oceans, Europa and Enceladus have emerged as two of the most promising targets in the search for extraterrestrial microbial life (Lunine 2017). The surfaces of these ice crusts are severely cold (e.g., -173°C on Europa; Wolfenbarger et al. 2022b), well below any temperature found on Earth, including during a Snowball Earth event. Yet temperatures permissive to Earth life are found in the lower portion of the linear gradient that exists in Europa's ice, from the surface to the ice-ocean interface (Wolfenbarger et al. 2022a). Both Europa and Enceladus have been modeled as having liquid reservoirs of ocean brine (even if the salt composition is poorly known) at interior locations within the ice crust, and Enceladus clearly expels material (gases, salt and ice particles, and organic compounds) into space through faults and fissures in the ice crust (Schmidt et al. 2011; see also figure 2 in Cockell et al. 2024). If an ocean below such a crust hosts microbial life (a big if), then the potential exists to find evidence of that life at some of the more accessible

<figure><img src="image_31.png" /></figure>
ice-liquid interfaces on these icy moons. Given the vertical gradients in sea ice on our planet, even if they are highly compressed compared with those on icy moons, sea ice and its inhabitants represent the best analogs we have for considering the possibility of life, and the possibility of detecting it, elsewhere in our solar system (Deming & Eicken 2007, Martin & McMinn 2018).

Wolfenbarger et al. (2022a) applied data on the limits of microbial life in sea ice, the extracellular products they release into their briny microhabitats, and the temperature-driven physical-chemical constraints on those brine inclusions (particularly water activity, ionic strength, and salinity) to a modeled ice crust on Europa. In developing habitability metrics for an ice thickness of 10 km, they considered the upper 80% of the ice to be uninhabitable but also to have the potential to contain relict life or biosignatures. Any possible liquid entering this region would have vitrified (flash frozen to a glassy state) given the severe temperatures. In the complete absence of liquid water, no metabolic activity could be expected, but bacterial cells, especially when surrounded by EPS, are known to preserve well when vitrified (Fahy & Wowk 2015). Organic preservation by vitrification suggests the potential to find biosignatures in this upper region of the ice crust. Below this relict region (Wolfenbarger et al. 2022a), the lower 20% of the ice was above the eutectic point and thus considered to contain brine inclusions. Except near the ice-ocean interface, these inclusions would be closed to nutrient or other exchanges. This nutrient-closed region could support metabolizing cells, as demonstrated in winter sea ice (Junge et al. 2004), but for a largely unknown period of time (Ewert et al. 2025). In the last meters of this modeled ice crust, and especially near the ice-water interface, brine inclusions would be open to exchange with the ocean below, as in Earth sea ice. In this nutrient-open region, microbial life could be supported and even flourish if the chemical nature of the ocean water is permissive. Many ifs figure in such modeled scenarios, but this line of inquiry demonstrates how knowledge of sea ice and its microbial inhabitants on our planet can help to inform the search for life elsewhere.

## DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.

## ACKNOWLEDGMENTS

We acknowledge support from the Aage V. Jensen Foundations and the Danish National Research Foundation (DNRF 185) (to S.R.) and the Karl M. Banse Endowed Professorship (to J.W.D.). E.M. is supported by the French National Research Agency [Agence Nationale de la Recherche (ANR)] (GRAL Labex ANR-10-LABEX-04, EUR CBS ANR-17-EURE-0003, CDP Glyco@Alps ANR-15-IDEX-0002, and Alpalga ANR-20-CE02-0020) and the Kilian Jornet Foundation. M.B. and E.M. are supported by ANR (DIM ANR-21-CE02-0021) and the Human Frontier Science Program (Trapped in Ice; http://doi.org/10.52044/HFSP.RGP0012024.pc.gr.194145). M.B. was also supported by the Sentinel North program. We are grateful to Linda Sohl, Susannah Porter, Warwick Vincent, and Anne Jungblut for the suggestions they made to improve this article.

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