PERSPECTIVE What Is Microbial Community Ecology?

PERSPECTIVE What Is Microbial Community Ecology?

The ISME Journal (2009) 3, 1223–1230 & 2009 International Society for Microbial Ecology All rights reserved 1751-7362/09 $32.00 www.nature.com/ismej PERSPECTIVE What is microbial community ecology? Allan Konopka Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, USA The activities of complex communities of microbes affect biogeochemical transformations in natural, managed and engineered ecosystems. Meaningfully defining what constitutes a community of interacting microbial populations is not trivial, but is important for rigorous progress in the field. Important elements of research in microbial community ecology include the analysis of functional pathways for nutrient resource and energy flows, mechanistic understanding of interactions between microbial populations and their environment, and the emergent properties of the complex community. Some emergent properties mirror those analyzed by community ecologists who study plants and animals: biological diversity, functional redundancy and system stability. However, because microbes possess mechanisms for the horizontal transfer of genetic information, the metagenome may also be considered as a community property. The ISME Journal (2009) 3, 1223–1230; doi:10.1038/ismej.2009.88; published online 6 August 2009 Keywords: microbial community; functional redundancy; microbial interactions; emergent properties Introduction will deepen our understanding of how ecosystems function. In turn, this understanding may elucidate Analyses of 16S rRNA gene sequences from envir- novel interaction mechanisms among multiple species onmental DNA have shown the extraordinary rich- at the single cell level (O’Malley and Dupre, 2007). ness of phylogenetic types found in many microbial There is great interest in applying modern habitats (Ley et al., 2006; Walker and Pace, 2007). As technologies in genome-enabled biology and analy- microbial ecologists have learned more about ‘who’s tical chemistry to concurrently study both the there,’ it has heightened interest in understanding identity and the function of complex microbial ‘what are they doing.’ The concerted activity of communities (DeLong et al., 2006; Musat et al., interacting microbes was critical to the development 2008). However, effective application requires a of environmental conditions on Earth that led to the clear delineation of what is meant by a ‘microbial evolution of multicellular organisms, and their community’ and identification of important catalysis of biogeochemical reactions has a central characteristics specific to community ecology. function in sustaining conditions that are compa- tible with a robust and diverse biosphere. At a time in which human beings are concerned with histori- cally rapid global change, understanding the control What is a microbial community? mechanisms whereby microbial communities deter- The concept of community ecology arose in plant mine ecosystem function is particularly relevant. and animal ecology. Communities are defined as Current ecosystem simulation models do not in- multi-species assemblages, in which organisms live clude microbial composition, and often neither together in a contiguous environment and interact explicitly consider the effects of environmental con- with each other. This discipline seeks to analyze ditions on microbial activities nor the interactions how biological assemblages are structured, what are between diverse microbial processes (Bardgett et al., their functional interactions and how community 2008). As microbial communities are of primary structure changes in space and time. Clements importance in biogeochemical transformations, a (1916) viewed the community as a ‘supra-organism’, deeper understanding of their dynamics will be which had a well-defined level of organization with critical to refined predictions regarding how the tight interactions among organisms that comprise a biosphere modulates and responds to future causal system and gives rise to emergent properties. environmental conditions. At a more fundamental The boundaries of the community may have less to level, understanding natural microbial communities do with physical dimensions than the range over which there are strong rather than weak interactions between populations (Levins and Lewontin, 1985). Correspondence: A Konopka, Biological Sciences Division, Pacific Northwest National Laboratory, PO Box 999, MSIN The alternative individualistic concept (Gleason, P7-50, Richland, WA 99352, USA. 1926) is that many species co-occur in a habitat E-mail: [email protected] because they tolerate similar physical and chemical Microbial community ecology A Konopka 1224 conditions and do not necessarily interact with each cannot be defined without reference to its abiotic other. The practical delineation of ‘community’ may environment. An appreciation for the tight inter- then reflect the interests of the ecologist rather than relationship between microbes and their microscale any inherent characteristics. physical and chemical environments is particularly The problems in rigorously defining community are important for delineation of microbial communities heightened in the case of microbial ecology. In (O’Donnell et al., 2007). In this spirit, it may be particular, delineating a ‘contiguous environment’ instructive to define microbial communities not and the meaning of ‘interact’ may be problematic. from a macroscale perspective (for example aquatic Microorganisms react to and in turn influence condi- vs terrestrial habitats), but rather based on a bottom- tions in their microenvironments, which usually have up analysis of the physicochemical characteristics length scales of microns rather than millimeters of the microenvironment, with upscaling to a spatial (Young et al., 2008), except in cases of multicellular domain (the ‘contiguous environment’) defined by structures such as fungal hyphae. However, the the region over which substantial direct interactions consumption of substrates and production of meta- or indirect chemical interactions are occurring. This bolic products in water-saturated sediments and approach presupposes adequate analysis of the local density-stabilized aquatic water columns can generate physicochemical environment, but technical inno- chemical gradients over meters (Wakeham et al., vations are moving to the microscale level (Young 2007). The consequence is that these functional et al., 2008). Konopka (2006) defined four ecosys- groups metabolically ‘interact’ over many meters. As tems derived by considering the environment from aresult,thestrengthofinteraction among organisms the microbe’s local perspective (Table 1). Each has and the defined spatial scale may vary substantially particular characteristics that define important for investigator-defined microbial communities. selective forces in that habitat, but which also To increase rigor in the meaning of ‘microbial impact the spatial scale over which microbial community,’ it would be valuable for microbial interactions occur. ecologists to explicitly articulate their meaning for each specific research effort. Microbes strongly interacting with each other in a microenvironment Elements of microbial community analysis comprise a local community. However, the distribu- tion of organisms and physicochemical properties Beyond the rigorous definition of a microbial within most habitats is patchy; even in apparently community, there remains the elucidation of its well-mixed oligotrophic planktonic habitats, nutri- essential characteristics. Levin (1999) proposed that ent-rich foci of marine snow may occur (Azam and ‘the most important challenge for ecologists remains Malfatti, 2007). The patchwork of local communities to understand the linkages between what is going on has been termed as a phenomenological community at the level of the physiology and behavior of (Sterelny, 2006); for the purposes of microbial individual organisms and emergent properties such ecology, this would represent a range of macroscale as the productivity and resiliency of ecosystems.’ habitats delineated by the investigator, in which the From this perspective, important elements for assemblage of microbes persists in spatial associa- analysis of microbial communities comprise fluxes, tion. The phenomenological community could be interactions and properties. constrained to a smaller number of populations by defining an indexical community—the set of popu- lations that directly interact with a key population Analysis of community functional pathways or defined biogeochemical process, together with Microbial communities provide ecosystem services other local populations that affect the directly (Ducklow, 2007) through the catalysis of biogeo- interacting populations (Sterelny, 2006). chemical reactions. Many reactions in chemoheter- Recent developments in community ecology have otrophs entail conversion of chemical elements from begun to recognize that the biological assemblage organic forms to inorganic forms that can be used by Table 1 Microbial-scale ecosystems Ecosystem type Examples Characteristics Planktonic Open ocean, lakes ‘Oligotroph lifestyle’. High affinity for uptake of multiple nutrients. Surface-associated, Freshwater and ocean sediments, ‘Gradient lifestyle’. Hydrodynamic processes and fluid saturated water subsurface sediments, microbial flow determine nutrient fluxes. Biomass density affects gradient mats, biofilms steepness. Surface-associated, Surface and vadose zone soils Water availability as limiting factor

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