# Editorial: Microbial Landscape Ecology: Highlights on the Invisible Corridors

Cendrine Mony, Brendan J. M. Bohannan, Mathew A. Leibold, Kabir Peay, Philippe Vandenkoornhuyse

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Cendrine Mony, Brendan J. M. Bohannan, Mathew A. Leibold, Kabir Peay, Philippe Vandenkoornhuyse. Editorial: Microbial Landscape Ecology: Highlights on the Invisible Corridors. Frontiers in Ecology and Evolution, 2021, 9, pp.753213. 10.3389/fevo.2021.753213. hal-03420429

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# Editorial: Microbial Landscape Ecology: Highlights on the Invisible Corridors

Cendrine Mony<fnref n="1" />*, Brendan J. M. Bohannan², Mathew A. Leibold³, Kabir Peay⁴ and Philippe Vandenkoornhuyse<fnref n="1" />

**Keywords:** landscape ecology, spatial ecology, metacommunity, assembly rule, microorganisms

## Editorial on the Research Topic

### Microbial Landscape Ecology: Highlights on the Invisible Corridors

## INTRODUCTION

Understanding community assembly is a key question in ecology (Kraft and Ackerly, 2014). The first integration of spatial processes at large spatial scales was introduced via the island biogeography theory of MacArthur and Wilson (1967), while landscape ecology emerged in the early 1990's as a new way for analyzing the causes and consequences of spatial patterns across landscapes (Wiens et al., 1993; Turner et al., 2001). In parallel, the consideration of species dynamics as resulting from the interrelationships among local populations, and individual fluxes among them led to the metapopulation concept (Hanski, 1994), extended 20 years ago to the metacommunity concept (Leibold et al., 2004). This framework based on a more mechanistic understanding of species distribution does not integrate space in an explicit manner, but considers dispersal fluxes as a proxy for population isolation. These two main conceptual streams have converged recently to allow better prediction of community assembly at the landscape level.

The application of these concepts to microbes has been slow to develop, due to our limited understanding of microbial habitat requirements, the species concept used, and our limited capacity for spatially extensive surveys of microbial distributions. In addition, there is a long-held assumption that microbial taxa have no meaningful dispersal limits because of their small size and high propagule production (Baas-Becking's hypothesis; Baas Becking, 1934). If unlimited passive dispersion of microorganisms is occurring, biotic and abiotic environmental filters would explain the observed high heterogeneity in the microbial communities in many (all) ecosystems. These views have been challenged by more recent evidence demonstrating strong dispersal limitation, and biogeography has consequently become more prominently used for describing and understanding large-scale spatial patterns (Martiny et al., 2006; Hanson et al., 2012; Donaldson et al., 2016).

Understanding the landscape-level drivers of microbiota complexity is important in a broader ecological context because of the tremendous role these microorganisms play in many ecological functions (e.g., carbon and nutrient cycles, resistance of organisms to stresses, behaviors, and reproduction, etc.). Despite the limitation of mass sequencing approaches in species detection, their application has resulted in the observation that microbial communities encompass tremendous taxonomic diversity, including bacteria, archaea, fungi, and protozoa. The microbial world is also characterized by a large range of life-styles, from free-living organisms to microorganisms associated with plant, animal, and human hosts. Landscape drivers may shape community assembly

**OPEN ACCESS**

Edited and reviewed by:
Peter Convey,
British Antarctic Survey (BAS),
United Kingdom

*Correspondence:
Cendrine Mony
cendrine.mony@univ-rennes1.fr

**Specialty section:**
This article was submitted to Biogeography and Macroecology, a section of the journal Frontiers in Ecology and Evolution

**Received:** 04 August 2021
**Accepted:** 30 August 2021
**Published:** 01 October 2021

**Citation:**

**Mony C, Bohannan BJM, Leibold MA, Peay K and Vandenkoornhuyse P**
(2021) *Editorial: Microbial Landscape Ecology: Highlights on the Invisible Corridors*. *Front. Ecol. Evol.* 9:753213.

doi: 10.3389/fevo.2021.753213

<footnote n="1">¹ Université de Rennes 1, CNRS, UMR6553 ECOBIO, Rennes, France, ² Center for Ecology and Evolutionary Biology, University of Oregon, Eugene, OR, United States, ³ Department of Biology, University of Florida, Gainesville, FL, United States, ⁴ Department of Biology, Stanford University, Stanford, CA, United States</footnote>
either directly through metapopulation and metacommunity
processes or indirectly through host-distribution, although these
relationships and their related mechanisms are still poorly
characterized, and have mostly focused on pathogens.

Overall the present topic addressed how landscape ecology
including metapopulation and metacommunity frameworks
can apply successfully to microorganisms. Through a large
range of microorganism types and ecosystems considered, we
provide a set of papers in this emerging field of microbial
landscape ecology. These are categorized in three main topics:
biogeography, landscape ecology, and metacommunity ecology.
A review of this existing state of the art and introduction to main
concepts are presented in this topic in *Mony et al.*

BIOGEOGRAPHY

Microorganisms are highly heterogeneous in space from large
to small spatial scales (e.g., Bahram et al., 2015). Biogeography
analyzes the spatial patterns at large scale and aims at
determining the environmental factors shaping these spatial
patterns. The development of biogeography for microorganisms
is recent (e.g., Martiny et al., 2006), applying both to terrestrial
microbes and aquatic microbes mostly at large spatial scales
of continents or regions. Drivers underlying spatial patterns
are investigated, and generally correspond to changes in abiotic
conditions (i.e., habitat characteristics). In the present topic,
Mukhtar et al. demonstrate strong environmental filtration of
microorganisms associated with plants suggesting a patchiness
being strongly dependent on selection processes. Integrating
space into account, Steven et al. demonstrated patchy distribution
of bacterial communities in the soil due to local habitat
distribution but also as a result of past disturbance. This article
nicely demonstrates the scale of response of these communities
both in space and time, and proposes that soil edaphic factors,
climatic disturbances, and physical trampling are drivers of
these biogeographical patterns. This article also provides an
interesting example of integrating drivers occurring in the past
for taking into account time-lags in species responses observed.
One key question related to understanding species patterns
concerns the possible local adaptation to patchy environments.
Wang et al. reported here geographical variation of mineral
elements of one cyanobacteria developing in the soil. This
article proposes to study both the geographical variation of one
microorganism species, and the related biochemical composition
and mineral element contents. This original work helps to
explore how the geographical variation of mineral content
promotes the ecological adaptation of soil cyanobacteria. In
most existing literature, biogeography has been applied at a
large spatial scale, Schiro et al. present here a demonstration
that biogeography can apply a very small spatial scale (scale
of a field). They demonstrated the small-scale heterogeneity
in fungi occurring in plant phyllosphere (and especially
pathogens). This heterogeneity was described by local taxon-level
selection to variable canopy environmental conditions, especially
linked to climatic conditions, but also to a lesser extent by
geographical position.

LANDSCAPE ECOLOGY

Landscape ecology provides a range of theories for understanding
how landscape structure affects species coexistence. Methods
specific to landscape ecology have been also developed to
precisely characterize landscape metrics, analyze how landscape
shapes species distribution and dispersal. Applications to
microorganisms have mostly focused on one species of interest
at a time, primarily pathogens (leading to the field of "landscape
epidemiology"). Landscape epidemiology has been developed
in all ecosystems on plant, animal or human pathogens, and
even within the human body for predicting the development
of infectious agents [see reviews of Holdenrieder et al. (2004)
and Suzan et al. (2012)]. Use of landscape ecology concepts
and methods in microbiology is at an early stage (see review
of Mony et al.). In this topic, Mennicken et al. proposed
an interesting study analyzing a recent theory of landscape
ecology, the habitat amount hypothesis (Fahrig, 2013), on a
large set of microorganism guilds and demonstrated for some
of them the importance of forest cover in the landscape.
Additionally, this article brings original evidence of time-lagged
dispersal processes, by demonstrating that patch age affects
the response of microorganisms to habitat amount. Integrating
time into landscape studies offers new promising prospects in
microbial ecology.

METACOMMUNITY ECOLOGY

Understanding the mechanisms of community assembly at
landscape spatial scales is a key issue. The metacommunity
framework assumes that community assembly results from four
key processes: dispersal, species sorting, patch dynamics, and
drift (Leibold et al., 2004). Metacommunity theory is a useful
framework for predicting species coexistence, as illustrated in
two articles in the topic. Zha et al. analyze how environmental
selection, dispersal, and drift explain variation in composition of
gut microbiota in fishes. In another study, Sokol et al. analyzed
the metacommunity functioning of diatoms in Antarctica, and
similarly demonstrated the effect of dispersal and species sorting
in community assembly. Because many microorganisms have
very short generation times, they are possibly experiencing more
rapid evolutionary processes than macroorganisms. Integrating
evolutionary processes in metacommunity models, O'Connor
et al. analyze evolutionary rescue within a metacommunity
framework and demonstrate that the history of antibiotic
selection and dispersal modes influence diversification in
microbial metacommunities. Metacommunity and landscape
ecology are generally poorly linked (Almeida-Gomes et al.,
2020), even in macroorganisms. Miller and Bohannan propose
an adaptation of the metacommunity model that takes into
account the permeability of the matrix to dispersal movement.
Using this adapted model, they analyzed how species traits
in microorganisms might promote species persistence in the
matrix, with possible adaptation to human and animal-associated
microbiomes. This study is a pioneering attempt to go beyond
the patch-matrix binary vision of landscape and to integrate
landscape heterogeneity into the metacommunity framework.
PERSPECTIVES

Integrating landscape-scale drivers in community assembly for microorganisms is an important step toward a better understanding of species distribution, although the application of landscape ecology is still in its infancy. The application of landscape ecology to microorganisms has a number of potential applications, including in environmental restoration (such as that described by Gonçalves Selari et al. in this special feature).

The *Mony et al.* review provides examples of how theories and methods from landscape ecology can be applied successfully to microbes; importantly, it also highlights the knowledge gaps that interfere with such application, including our ignorance of many ecological processes operating at the landscape scale, such as microbial dispersal. It also stresses the need for adaptation of this framework to take into account microorganism characteristics and better integration of their real dispersion rates and realized niches. Landscape-microbe relationships are more complex, and less well-understood, than for macroorganisms involving a large range of response scales—from the classical landscape scale to micro landscapes—, nested spatial and temporal scales, and a unique case of biotic landscapes for host-associated microorganisms. Microbial community composition and distribution are also often driven directly by their host distribution, and feedback loops between micro- and macro-organisms likely occur. If the landscape ecology framework in its broad sense (i.e., including biogeography and metacommunity concepts) provides a new avenue for testing ecological hypotheses

on microbial community assembly, along with eco-evolutionary processes shaping communities, microbes provide also a unique and original case study that might considerably enrich the existing theoretical backgrounds and methods. Within a more holistic framework of understanding the application of landscape ecology to the microbial world is susceptible to modify our understanding not solely about the rules of microbial community assembly, but also for instance (i) eco-evolutionary processes and dynamics structuring microbial communities, (ii) macro-ecological processes resulting from changes of microbial communities, (iii) links between host and symbionts, all resulting from/to a better interpretation to which extend the neutral model of assembly is applicable rather than non-random influences of niche differentiation to the considered microbial community. The landscape of opportunities for future research in this field is wide.

AUTHOR CONTRIBUTIONS

CM wrote the first draft. All authors reviewed the text and gave final approval.

FUNDING

This research was funded by U.S. NSF award 2025118 (to ML), CNRS EC2CO (to PV), and l'agence Française pour la Biodiversité project AGRIM (to CM).

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**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.

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