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A Landscape of Opportunities for Microbial Ecology Research Cendrine Mony, Philippe Vandenkoornhuyse, Brendan J

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A Landscape of Opportunities for Microbial Ecology Research Cendrine Mony, Philippe Vandenkoornhuyse, Brendan J A Landscape of Opportunities for Microbial Ecology Research Cendrine Mony, Philippe Vandenkoornhuyse, Brendan J. M. Bohannan, Kabir Peay, Mathew A. Leibold To cite this version: Cendrine Mony, Philippe Vandenkoornhuyse, Brendan J. M. Bohannan, Kabir Peay, Mathew A. Leibold. A Landscape of Opportunities for Microbial Ecology Research. Frontiers in Microbiology, Frontiers Media, 2020, 11, pp.a561427. 10.3389/fmicb.2020.561427. hal-03095745 HAL Id: hal-03095745 https://hal.archives-ouvertes.fr/hal-03095745 Submitted on 4 Jan 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License fmicb-11-561427 November 18, 2020 Time: 14:54 # 1 REVIEW published: 20 November 2020 doi: 10.3389/fmicb.2020.561427 A Landscape of Opportunities for Microbial Ecology Research Cendrine Mony1*, Philippe Vandenkoornhuyse1, Brendan J. M. Bohannan2, Kabir Peay3 and Mathew A Leibold4 1 UMR CNRS ECOBIO, Université de Rennes, Rennes, France, 2 Institute of Ecology and Evolution, University of Oregon, Eugene, ORE, United States, 3 Department of Biology, University of Stanford, Stanford, CA, United States, 4 Department of Biology, University of Florida, Gainesville, FL, United States Microbes encompass tremendous biodiversity, provide support to all living forms, including humans, and play an important role in many ecosystem services. The rules that govern microorganism community assembly are increasingly revealed due to key advances in molecular and analytical methods but their understanding remain a key challenge in microbial ecology. The existence of biogeographic patterns within microbial communities has been established and explained in relation to landscape- scale processes, including selection, drift, dispersal and mutation. The effect of Edited by: habitat patchiness on microorganisms’ assembly rules remains though incompletely Eoin L. Brodie, understood. Here, we review how landscape ecology principles can be adapted to Lawrence Berkeley National explore new perspectives on the mechanisms that determine microbial community Laboratory, United States structure. To provide a general overview, we characterize microbial landscapes, the Reviewed by: Alban Ramette, spatial and temporal scales of the mechanisms that drive microbial assembly and University of Bern, Switzerland the feedback between microorganisms and landscape structure. We provide evidence Kimberley Warren-Rhodes, Ames Research Center, National for the effects of landscape heterogeneity, landscape fragmentation and landscape Aeronautics and Space dynamics on microbial community structure, and show that predictions made for Administration (NASA), United States macro-organisms at least partly also apply to microorganisms. We explain why *Correspondence: emerging metacommunity approaches in microbial ecology should include explicit Cendrine Mony [email protected] characterization of landscape structure in their development and interpretation. We also explain how biotic interactions, such as competition, prey-predator or mutualist relations Specialty section: may influence the microbial landscape and may be involved in the above-mentioned This article was submitted to Terrestrial Microbiology, feedback process. However, we argue that the application of landscape ecology to a section of the journal the microbial world cannot simply involve transposing existing theoretical frameworks. Frontiers in Microbiology This is due to the particularity of these organisms, in terms of size, generation time, Received: 12 May 2020 Accepted: 30 October 2020 and for some of them, tight interaction with hosts. These characteristics imply dealing Published: 20 November 2020 with unusual and dependent space and time scales of effect. Evolutionary processes Citation: have also a strong importance in microorganisms’ response to their landscapes. Lastly, Mony C, Vandenkoornhuyse P, microorganisms’ activity and distribution induce feedback effects on the landscape that Bohannan BJM, Peay K and Leibold MA (2020) A Landscape have to be taken into account. The transposition of the landscape ecology framework of Opportunities for Microbial Ecology to microorganisms provides many challenging research directions for microbial ecology. Research. Front. Microbiol. 11:561427. Keywords: landscape ecology, metacommunity, microbial assembly-rules, dispersal, plant microbiota, human doi: 10.3389/fmicb.2020.561427 microbiota, animal microbiota Frontiers in Microbiology| www.frontiersin.org 1 November 2020| Volume 11| Article 561427 fmicb-11-561427 November 18, 2020 Time: 14:54 # 2 Mony et al. Landscape Ecology Applied to Microbes INTRODUCTION (including both abiotic and biotic factors), speciation (analogous to mutation in population genetics), dispersal and ecological drift Microorganisms represent by far the largest fraction of (Box 1; Vellend, 2010, 2016). biodiversity (Curtis and Sloan, 2005). There are 100 million An alternative approach to spatial dynamics in ecology times as many bacteria in the oceans (13 × 1028) as there emerged some 30 years ago in the form of landscape ecology are stars in the known universe [:::] [Editorial Nature Reviews (Wiens et al., 1993; Turner et al., 2001; Fletcher and Fortin, in Microbiology, (No authors listed, 2011)]. The amazing 2018). Landscape ecology focused specifically on the explicit abundance of microorganisms on earth plays a central role analysis of spatial ecological patterns and has determined the in the biogeochemical cycles of elements (Curtis and Sloan, conceptualization of what a landscape is (Figure 2), and provided 2005), affects soil fertility, organic matter decomposition and tools for analyzing how spatial processes influenced the assembly carbon storage. Microorganisms are also required to sustain of biodiversity, focusing primarily on plants and animals (Box all living macroorganisms, including humans (Curtis, 2006), as 1). Landscape structure, described through different metrics they are involved in the nutrition, health, reproduction and at the landscape scale (i.e., heterogeneity) or the habitat scale behavior of their hosts (Curtis, 2006; Boulangé et al., 2016; (i.e., fragmentation), has been shown to affect dispersal, and Vuong et al., 2017). They consequently ensure the majority local habitat exploitation during an organism’s lifecycle, but of ecosystem services provided to our society (Philippot et al., also the availability of habitat for species development and 2013; Vandenkoornhuyse et al., 2015). However, microorganisms movements among local patches (Figure 3 and Box 1). These display a substantial spatial heterogeneity (Box 1, see reviews two types of metrics - landscape heterogeneity and fragmentation Etterma and Wardle, 2002; Green and Bohannan, 2006; - affect species abundance and composition (Fahrig, 2003). Franklin and Mills, 2007; Bahram et al., 2015). This raises Landscape ecology research has, however, mostly concentrated questions about how the distribution of microbes depends on on macroorganisms and the microbial compartment has different components of community assembly, its link with remained understudied under this framework. niche theory and coexistence mechanisms, and how community Applying landscape ecology principles to microorganisms assembly is linked to the functions and functioning of these has, until recently, been slow to develop due to our limited microbial ecosystems. understanding of microbial habitat requirements, the difficulties Drivers of microorganism assemblages have so far mostly been involved in observing microorganisms movements and our analyzed at the patch scale, assuming that species niches result limited capacity to conduct spatially extensive surveys of from the effect of the abiotic environment on species selection, microbial distribution. The determination of microbial disturbance or biotic interactions among microbial organisms community composition is also by itself difficult given that (Niche theory, Figure 1), or with their host (Louca et al., microbial communities can be quite complex and need 2018) and ignoring dispersal effects. Because microorganisms to be studied by mass-sequencing approaches. From the have very high reproductive capacities and short generation nature of the data used, the microbial species-sequence time, the historical view “everything is everywhere but the delineation is also needed and the adoption of a phylogenetic environment selects”(Baas Becking, 1934) has been accepted species concept (i.e., “[...] the smallest diagnosable cluster for a long time. The progress in resolution of microbial of individual organisms within which there is a pattern communities composition obtained from mass sequencing and of ancestry and descent. [...]” (Cracraft, 1983)) is implicit. large-scale studies of microbial distribution (see for instance After having used cutoff of sequence identity to identify Karimi et al., 2018) provided an increased number of evidences Operational Taxonomic Units, recent bioinformatics advances that microorganisms are
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