Understanding how microbiomes influence the systems they inhabit

Translating the ever-increasing wealth of information on microbiomes (environment, host or built environment) to advance our understanding of system-level processes is proving to be an exceptional research challenge. One reason for this challenge is that relationships between characteristics of microbiomes and the system-level processes that they influence are often evaluated in the absence of a robust conceptual framework and reported without elucidating the underlying causal mechanisms. The reliance on correlative approaches limits the potential to expand the inference of a single relationship to additional systems and advance the field. We propose that research focused on how microbiomes influence the systems they inhabit should work within a common framework and target known microbial processes that contribute to the system-level processes of interest. Here, we identify three distinct categories of microbiome characteristics (microbial processes, microbial community properties and microbial membership) and propose a framework to empirically link each of these categories to each other and the broader system-level processes that they affect. We posit that it is particularly important to distinguish microbial community properties that can be predicted using constituent taxa (community-aggregated traits) from those properties that cannot currently be predicted using constituent taxa (emergent properties). Existing methods in microbial ecology can be applied to more explicitly elucidate properties within each of these three categories of microbial characteristics and connect them with each other. We view this proposed framework, gleaned from a breadth of research on environmental microbiomes and ecosystem processes, as a promising pathway with the potential to advance discovery and understanding across a broad range of microbiome science.This Review Article discusses the importance of considering known microbial processes to inform our understanding of the role of microbial communities in ecosystem processes, and a move away from approaches based solely on correlation analyses.

[1]  P. Bodelier Interactions between nitrogenous fertilizers and methane cycling in wetland and upland soils , 2011 .

[2]  G. Kling,et al.  Metacommunity dynamics of bacteria in an arctic lake: the impact of species sorting and mass effects on bacterial production and biogeography , 2014, Front. Microbiol..

[3]  Roberto Danovaro,et al.  Simultaneous Recovery of Extracellular and Intracellular DNA Suitable for Molecular Studies from Marine Sediments , 2005, Applied and Environmental Microbiology.

[4]  N. Fierer,et al.  Biological Diversity and Function in Soils: Microbial community composition and soil nitrogen cycling: is there really a connection? , 2005 .

[5]  S. Chisholm,et al.  Prochlorococcus: the structure and function of collective diversity , 2014, Nature Reviews Microbiology.

[6]  M. Wagner Single-cell ecophysiology of microbes as revealed by Raman microspectroscopy or secondary ion mass spectrometry imaging. , 2009, Annual review of microbiology.

[7]  Steven D. Allison,et al.  The Michaelis–Menten kinetics of soil extracellular enzymes in response to temperature: a cross‐latitudinal study , 2012 .

[8]  J. R. van der Meer,et al.  Use of flow cytometric methods for single-cell analysis in environmental microbiology. , 2008, Current opinion in microbiology.

[9]  J. Schimel Ecosystem Consequences of Microbial Diversity and Community Structure , 1995 .

[10]  S. Allison,et al.  Elemental stoichiometry of Fungi and Bacteria strains from grassland leaf litter , 2014 .

[11]  M. Wallenstein,et al.  A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning , 2012, Biogeochemistry.

[12]  J. C. Goldman,et al.  Regulation of gross growth efficiency and ammonium regeneration in bacteria by substrate C: N ratio1 , 1987 .

[13]  Jay T. Lennon,et al.  Microbiomes in light of traits: A phylogenetic perspective , 2015, Science.

[14]  Kai Zhu,et al.  Individual-scale variation, species-scale differences: inference needed to understand diversity. , 2011, Ecology letters.

[15]  P. Reich,et al.  Diversity and Productivity in a Long-Term Grassland Experiment , 2001, Science.

[16]  Davey L. Jones,et al.  Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes? , 2016, Front. Microbiol..

[17]  D. A. Klein Bulk Extraction-Based Microbial Ecology: Three Critical Questions , 2011 .

[18]  W. Wieder,et al.  Do we need to understand microbial communities to predict ecosystem function? A comparison of statistical models of nitrogen cycling processes , 2014 .

[19]  J. L. Green,et al.  A unified initiative to harness Earth's microbiomes , 2015, Science.

[20]  Allan Konopka,et al.  What is microbial community ecology? , 2009, The ISME Journal.

[21]  M. Strickland,et al.  Considering fungal:bacterial dominance in soils – Methods, controls, and ecosystem implications , 2010 .

[22]  J. Lennon,et al.  Microbial seed banks: the ecological and evolutionary implications of dormancy , 2011, Nature Reviews Microbiology.

[23]  R. Danovaro,et al.  Extracellular DNA Plays a Key Role in Deep-Sea Ecosystem Functioning , 2005, Science.

[24]  M. Usher,et al.  Biological diversity and function in soils. , 2005 .

[25]  E. Delong,et al.  The Microbial Engines That Drive Earth's Biogeochemical Cycles , 2008, Science.

[26]  M. Bradford,et al.  Microbial stoichiometry overrides biomass as a regulator of soil carbon and nitrogen cycling. , 2015, Ecology.

[27]  J. Lennon,et al.  Linking microbial community structure and microbial processes: an empirical and conceptual overview. , 2015, FEMS microbiology ecology.

[28]  Eoin L. Brodie,et al.  Toward a Predictive Understanding of Earth’s Microbiomes to Address 21st Century Challenges , 2016, mBio.

[29]  C. Körner,et al.  Arctic and Alpine Biodiversity: Patterns, Causes and Ecosystem Consequences , 1994, Ecological Studies.

[30]  Michaeline B. N. Albright,et al.  Function and functional redundancy in microbial systems , 2018, Nature Ecology & Evolution.

[31]  E. K. Hall,et al.  Linking Microbial and Ecosystem Ecology Using Ecological Stoichiometry: A Synthesis of Conceptual and Empirical Approaches , 2011, Ecosystems.

[32]  K. Treseder,et al.  Fungal Traits That Drive Ecosystem Dynamics on Land , 2015, Microbiology and Molecular Reviews.

[33]  G. Somero,et al.  Biochemical Adaptation: Mechanism and Process in Physiological Evolution , 1984 .

[34]  J. Newbold,et al.  Effects of Current Velocity on the Nascent Architecture of Stream Microbial Biofilms , 2003, Applied and Environmental Microbiology.

[35]  Josh D Neufeld,et al.  DNA stable-isotope probing , 2007, Nature Protocols.

[36]  Donald R Schoolmaster,et al.  Mapping the niche space of soil microorganisms using taxonomy and traits. , 2012, Ecology.

[37]  J. Lapierre,et al.  The quality of organic matter shapes the functional biogeography of bacterioplankton across boreal freshwater ecosystems , 2015 .

[38]  Katherine D. McMahon,et al.  A Guide to the Natural History of Freshwater Lake Bacteria , 2011, Microbiology and Molecular Reviews.

[39]  J. Lennon,et al.  Relationships between protein-encoding gene abundance and corresponding process are commonly assumed yet rarely observed , 2014, The ISME Journal.

[40]  J. Elser,et al.  Elemental ratios and the uptake and release of nutrients by phytoplankton and bacteria in three lakes of the Canadian shield , 1995, Microbial Ecology.

[41]  M. Heldal,et al.  Light element analysis of individual bacteria by x-ray microanalysis , 1995, Applied and environmental microbiology.

[42]  J. Comte,et al.  Links between metabolic plasticity and functional redundancy in freshwater bacterioplankton communities , 2013, Front. Microbiol..

[43]  J. G. Kuenen,et al.  Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor , 1995 .

[44]  Noah Fierer,et al.  Seeing the forest for the genes: using metagenomics to infer the aggregated traits of microbial communities , 2014, Front. Microbiol..

[45]  Peter E. Thornton,et al.  Carbon-nitrogen interactions regulate climate-carbon cycle feedbacks: results from an atmosphere-ocean general circulation model , 2009 .

[46]  M. Angilletta Thermal Adaptation: A Theoretical and Empirical Synthesis , 2009 .

[47]  R. B. Jackson,et al.  The Global Stoichiometry of Litter Nitrogen Mineralization , 2008, Science.

[48]  W. Wanek,et al.  The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency. , 2010, FEMS microbiology ecology.

[49]  J. Gilbert,et al.  Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus’ , 2016, Nature Microbiology.

[50]  K. Foster,et al.  Competition, Not Cooperation, Dominates Interactions among Culturable Microbial Species , 2012, Current Biology.

[51]  Andreas Kappler,et al.  Linking environmental processes to the in situ functioning of microorganisms by high-resolution secondary ion mass spectrometry (NanoSIMS) and scanning transmission X-ray microscopy (STXM). , 2012, Environmental microbiology.

[52]  J. Mikola Biological Diversity and Function in Soils , 2006 .

[53]  Brian C. Thomas,et al.  A new view of the tree of life , 2016, Nature Microbiology.

[54]  M. Pace,et al.  Regulation of planktonic bacterial growth rates: The effects of temperature and resources , 2004, Microbial Ecology.

[55]  G. Salt A Comment on the Use of the Term Emergent Properties , 1979, The American Naturalist.

[56]  B. Jørgensen,et al.  Origin, dynamics, and implications of extracellular DNA pools in marine sediments. , 2015, Marine genomics.

[57]  G. Odegard,et al.  Simulation of the Elastic and Ultimate Tensile Properties of Diamond, Graphene, Carbon Nanotubes, and Amorphous Carbon Using a Revised ReaxFF Parametrization. , 2015, The journal of physical chemistry. A.

[58]  M. Wagner,et al.  A ‘rare biosphere’ microorganism contributes to sulfate reduction in a peatland , 2010, The ISME Journal.

[59]  M. Facciotti,et al.  Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh , 2014, Environmental microbiology.

[60]  E. Casamayor,et al.  Contrasting activity patterns determined by BrdU incorporation in bacterial ribotypes from the Arctic Ocean in winter , 2013, Front. Microbiol..

[61]  James H. Brown,et al.  Microbial biogeography: putting microorganisms on the map , 2006, Nature Reviews Microbiology.

[62]  J. Russell The Energy Spilling Reactions of Bacteria and Other Organisms , 2007, Journal of Molecular Microbiology and Biotechnology.

[63]  F. Azam,et al.  Isolates as models to study bacterial ecophysiology and biogeochemistry , 2017 .

[64]  J. Grilli,et al.  Higher-order interactions stabilize dynamics in competitive network models , 2017, Nature.

[65]  C. Kammann,et al.  Evidence for methane production by saprotrophic fungi , 2012, Nature Communications.

[66]  Mark P. Simmons,et al.  Co-variation in methanotroph community composition and activity in three temperate grassland soils , 2016 .

[67]  C. Godwin,et al.  Stoichiometric flexibility in diverse aquatic heterotrophic bacteria is coupled to differences in cellular phosphorus quotas , 2015, Front. Microbiol..

[68]  Alyse A. Larkin,et al.  Microdiversity shapes the traits, niche space, and biogeography of microbial taxa. , 2017, Environmental microbiology reports.

[69]  J. Cotner,et al.  The effect of temperature on the coupling between phosphorus and growth in lacustrine bacterioplankton communities , 2009 .