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# Editorial: Deep subsurface microbiology and energetics

Alberto Robador, William J Brazelton, James Andrew Bradley

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Alberto Robador, William J Brazelton, James Andrew Bradley. Editorial: Deep subsurface microbiology and energetics. Frontiers in Microbiology, 2025, 16, 10.3389/fmicb.2025.1611707. [https://doi.org/10.3389/fmicb.2025.1611707](https://doi.org/10.3389/fmicb.2025.1611707). [CC-BY](https://creativecommons.org/licenses/by/4.0/)

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Submitted on 27 Jul 2025

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OPEN ACCESS

EDITED AND REVIEWED BY

Andreas Teske,
University of North Carolina at Chapel Hill,
United States

*CORRESPONDENCE

Alberto Robador

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robadora@usc.edu

RECEIVED 14 April 2025

ACCEPTED 21 April 2025

PUBLISHED 07 May 2025

CITATION

Robador A, Brazelton WJ and Bradley JA
(2025) Editorial: Deep subsurface
microbiology and energetics.

Front. Microbiol. 16:1611707.

doi: 10.3389/fmicb.2025.1611707

COPYRIGHT

© 2025 Robador, Brazelton and Bradley. This
is an open-access article distributed under the
terms of the [Creative Commons Attribution
License (CC BY)](https://creativecommons.org/licenses/by/4.0/).
The use, distribution or
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No use, distribution or reproduction is
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Editorial: Deep subsurface
microbiology and energetics

Alberto Robador<fnref n="1" />*, William J. Brazelton<fnref n="2" /> and
James Andrew Bradley<fnref n="3" />

KEYWORDS

deep biosphere, microbial energetics, redox zonation, energy-limiting ecosystems, subsurface biogeochemistry

Editorial on the Research Topic

Deep subsurface microbiology and energetics

Introduction

Deep subsurface environments host vast and dynamic ecosystems that challenge conventional paradigms of the rules of microbial life. At the same time, these unusual ecosystems are integral to Earth's biogeochemical cycles. Because these environments are shaped by geological processes and often constrained by extreme energetic limitations, life in the deep subsurface is governed by complex interactions among redox chemistry, spatial structure, and long-term adaptation to energy scarcity. The collection of articles presented in this Research Topic, "*Deep subsurface microbiology and energetics*," provides an interdisciplinary perspective through which to examine the metabolic potential, ecological organization, and functional resilience of microorganisms inhabiting these remote environments.

Redox zonation and microbial niche partitioning

Microbial metabolism in the deep subsurface is tightly coupled to redox gradients established by the interactions of water, rock and biology. These gradients define not only the thermodynamic constraints for energy conservation but also the spatial partitioning of microbial niches.

In hyperalkaline fluids derived from serpentinization in the Samail Ophiolite, *Howells et al.* reveal that formate, rather than hydrogen or acetate, provides the most favorable energy source for methanogenesis under CO₂-limiting conditions. This finding highlights the selective pressure exerted by fluid geochemistry on microbial metabolic strategies with the unusual example of CO₂ as the limiting substrate. In a related system, *Twing et al.* investigate microbial communities within altered ultramafic rocks from the Coast Range Ophiolite. Their results underscore the distinction between rock-hosted and fluid-associated microbial assemblages, with implications for potential spatial isolation and endemism of deep biosphere lineages.

Sedimentological and fracture-hosted systems offer further insights into the persistence
of microbial metabolic potential over time. In the sediments of Lake Cadagno,

<footnote n="1">¹Department of Biological Sciences, University of Southern California, Los Angeles, CA, United States,</footnote>

<footnote n="2">²School of Biological Sciences, The University of Utah, Salt Lake City, UT, United States,</footnote>

<footnote n="3">³Mediterranean Institute of Oceanography, Marseille, France</footnote>
Rodriguez et al. document the preservation of core metabolic
functions across millennia, despite taxonomic shifts in sediment
microbial communities. Similarly, Acciardo et al. report stable
groundwater microbial and hydrochemical compositions across
an Alpine tunnel system, in spite of notable temporary variations
corresponding to seismic events. These studies collectively
suggest that functional redundancy and environmental buffering
contribute to the resilience of deep subsurface microbiomes.

Strategies for survival in
energy-limited settings

Adaptation to energy scarcity is a hallmark of deep subsurface
systems. Survival in the energy-limited subsurface depends not only
metabolic versatility but also regulatory and genomic mechanisms
attuned to long-term energy deprivation and survival over
long timescales.

Sebastian et al. address this challenge through an experimental evolution framework, demonstrating that *Halomonas* strains isolated from North Pond crustal fluids rapidly lose the genetic capacity for survival in carbon-depleted media when exposed to nutrient-rich laboratory conditions. Their findings point to specific gene products, including lipase-like proteins, as key mediators of nutrient acquisition under oligotrophic conditions.

Complementing this genomic perspective, *Feyhl-Buska* et al. use microcalorimetry to directly quantify energy metabolism in groundwater samples spanning a range of redox conditions, revealing nutrient limitation in continental subsurface communities. The results provide empirical constraints on microbial power output and underscore the influence of both thermodynamic and ecological parameters on community-level metabolism.

Beyond classical metabolism: novel energetic pathways and functional innovation

Emerging theoretical frameworks and cultivation-based
discoveries continue to expand the known boundaries of
microbial energetics.

Karnachuk et al. describe the isolation of two novel
thermophilic bacterial genera from deep aquifers in Western
Siberia. These members of the *Limnochordia* lineage possess the
capacity for carbon monoxide and hydrogen oxidation, autotrophic
carbon fixation, and aerobic respiration. Their physiological
versatility illustrates the metabolic plasticity that may underpin
survival in thermally and chemically extreme environments.

A conceptual advance is presented by Marshall, who proposes the existence of Electromicrobiological Concentration Cells (EMCCs). These hypothetical systems rely on conductive matrices to bridge spatially distinct redox reactions, allowing microorganisms to exploit electrochemical disequilibria that would otherwise be inaccessible. The EMCC framework challenges traditional assumptions about the spatial coherence required for

microbial energy harvesting and may have relevance for life in both
deep terrestrial and extraterrestrial settings.

Coupled biogeochemical cycling and
ecosystem regulation

The influence of subsurface microbial communities extends
to the regulation of key geochemical processes, including
methane production and oxidation, nutrient turnover, and
mineral transformation.

Coon et al. demonstrate that the directionality of methane
cycling in coastal sediments is modulated by hydrogen availability.
In organic-poor settings, syntrophic interactions between
fermenters and methanogens or sulfate reducers maintain
low hydrogen concentrations, promoting fermentation and
anaerobic methane oxidation. Conversely, elevated hydrogen
levels in organic-rich sediments destabilize these interactions,
favoring methanogenesis.

In the context of engineered subsurface environments, Cheng et al. investigate microbial community dynamics in oil reservoir cores subjected to nutrient amendments. Their findings indicate that nutrient limitation supports greater community diversity and network stability, whereas nutrient enrichment promotes dominance by functionally narrow taxa and reduces ecological resilience.

This theme is extended by Mura et al., who simulate dihydrogen (H₂) co-injection in a natural gas-bearing, low-salinity deep aquifer under controlled laboratory conditions. Using a high-pressure reactor system with native rock and fluid phases, they show that microbial activity leads to sequential reduction processes, including sulfate reduction, acetogenesis, and ultimately methanogenesis, with the latter accounting for the majority of H₂ consumption. While microbial H₂ uptake remained limited—likely due to nutrient depletion—the work reveals that aquifers with low salinity and restricted electron acceptor availability may provide relatively stable reservoirs for H₂ storage. This study further emphasizes the need for site-specific microbial and geochemical assessment when evaluating the feasibility of underground H₂ storage.

Further advancing the discussion on trace element-driven
microbial processes, Montoya and Escobar-Briones explore the
role of cobalt and vitamin B12 (cobalamin) in structuring microbial
and metazoan communities associated with ferromanganese
crusts and polymetallic nodules. These cobalt-rich habitats host
diverse microbial assemblages, including cobalamin-producing
prokaryotes such as Thaumarchaeota and Proteobacteria, which
support cobalamin-auxotrophic eukaryotes via trophic and
symbiotic interactions. The authors argue that the abundance
of cobalt in these deep-sea mineral systems may create
micronutrient “hotspots” where metabolic interdependencies
become intensified. This framework posits cobalt and cobalamin
as pivotal drivers of deep-sea microbial ecology and proposes that
these mineral-rich habitats offer valuable models for studying
micronutrient-based ecological networks and their vulnerability to
anthropogenic disturbance.
# Integrating the deep subsurface biosphere into planetary systems thinking

A broader systems perspective is articulated by Robador, who conceptualizes the oceanic crustal biosphere as a globally distributed, low-energy biogeochemical reactor. This framework situates subseafloor microbial processes within Earth's carbon cycle and emphasizes the significance of subsurface ecosystems in global redox balance. By drawing parallels between deep biosphere functions and potential analogs on other planetary bodies, the review reinforces the role of subsurface microbiology in astrobiology and Earth system science.

## Concluding remarks

The contributions compiled in this Research Topic underscore the multifaceted nature of deep subsurface microbial life. From theoretical advances and empirical discoveries to environmental and engineered system analyses, these studies highlight the central role of microbial subsurface communities in mediating geochemical processes under extreme conditions. As exploration of subsurface environments continues—on Earth and beyond— the principles of microbial energetics, adaptation, and resilience described herein will serve as a foundation for understanding life in one of its most enigmatic domains.

This Research Topic is in memory of Jan Amend, whose work and ideas, mentorship, enthusiasm and leadership not only

transformed the field of deep subsurface microbiology but also inspired and guided a generation of scientists that have continued to advance this field.

## Author contributions

AR: Conceptualization, Writing – original draft, Writing – review & editing. WB: Writing – review & editing. JB: Writing – review & editing.

## Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

## Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.