Emerging Patterns of Microbial Functional Traits

To understand the cause of microbial community dynamics and ecosystem consequences, scientists must analyze the patterns of microbial functional traits under various environmental conditions and associate functional traits with ecosystem processes. Challenges in cultivation and trait measurement, lack of robust definition of microbial species, and ecological incoherence of the microbial world have disallowed the direct application of trait concepts and tools developed for macro-organisms. In addition to serving as next-generation biomonitoring tools for assessing environmental safety and health risks, microbial functional traits could be used to explain biogeochemical cycling and improve ecosystem modeling. More research programs are needed for generating a knowledge base of functional traits, a critical step for environmental biomonitoring and biogeochemical process modeling in a time of rapid global changes. Functional traits are measurable characteristics that affect an organism’s fitness under certain environmental conditions. The use of functional traits in microbial ecology holds great promise for improving our ability to develop biogeochemical models and predict ecosystem responses to global changes. Notably, functional traits could be decoupled from taxonomic relatedness, owing to horizontal gene transfer among microorganisms and adaptive evolution. In recent years, our knowledge about microbial functional traits has been substantially enhanced, thereby revealing the multitude of ecological processes in driving community assembly and dynamics. Here, I summarize the emerging patterns of how microbial functional traits respond to changing environments, which considerably differ from better-studied microbial taxonomy. I use niche and neutral theories to explain microbial functional traits. Finally, I highlight future challenges to analyze, elucidate, and utilize functional traits in microbial ecology. Functional traits are measurable characteristics that affect an organism’s fitness under certain environmental conditions. The use of functional traits in microbial ecology holds great promise for improving our ability to develop biogeochemical models and predict ecosystem responses to global changes. Notably, functional traits could be decoupled from taxonomic relatedness, owing to horizontal gene transfer among microorganisms and adaptive evolution. In recent years, our knowledge about microbial functional traits has been substantially enhanced, thereby revealing the multitude of ecological processes in driving community assembly and dynamics. Here, I summarize the emerging patterns of how microbial functional traits respond to changing environments, which considerably differ from better-studied microbial taxonomy. I use niche and neutral theories to explain microbial functional traits. Finally, I highlight future challenges to analyze, elucidate, and utilize functional traits in microbial ecology. a nonrandom mechanism in ecology that affects the biological community's patterns and behaviors [57.Stegen J.C. et al.Quantifying community assembly processes and identifying features that impose them.ISME J. 2013; 7: 2069-2079Crossref PubMed Scopus (580) Google Scholar]. In other words, a deterministic process is niche-based. Therefore, patterns and behaviors can be predicted by abiotic and biotic environmental factors. the phenomenon that members of a taxon do not share the same life strategies or functional traits with other members of the same taxon [18.Jaspers E. Overmann J. Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies.Appl. Environ. Microbiol. 2004; 70: 4831-4839Crossref PubMed Scopus (236) Google Scholar,19.Philippot L. et al.The ecological coherence of high bacterial taxonomic ranks.Nat. Rev. Microbiol. 2010; 8: 523-529Crossref PubMed Scopus (382) Google Scholar]. physical, chemical, and biological actions or events occurring in an ecosystem. the total abundance of a functional trait [2.Violle C. et al.Let the concept of trait be functional!.Oikos. 2007; 116: 882-892Crossref Scopus (2483) Google Scholar]. Relative functional abundance can be calculated from amplicon or metagenome sequencing data, while absolute functional abundance can be calculated by incorporating microbial biomass information. the proportions of a functional trait in individual organisms relative to the total population possessing the functional trait [2.Violle C. et al.Let the concept of trait be functional!.Oikos. 2007; 116: 882-892Crossref Scopus (2483) Google Scholar]. Functional composition is generally expressed as a percentage, so that all components add up to 100%. It is a guild or community-level variable. a community-level variable to indicate the degree of functional dissimilarity in trait values within a community, which is also termed as trait range or functional β-diversity. It can also be expressed as the number of functional groups, which takes into account both the number of functional groups and trait values within a functional group. Functional divergence emphasizes the presence of various functional traits attributed to ecological differences between species, which leads to complete utilization of resources, making it informative for ecosystem processes [7.de Bello F. et al.Towards an assessment of multiple ecosystem processes and services via functional traits.Biodivers. Conserv. 2010; 19: 2873-2893Crossref Scopus (600) Google Scholar]. the variability among functional traits. It includes functional α-diversity, which is calculated by either the richness of functional trait or Shannon and Simpson indices when taking account of trait abundance. It also includes β-diversity, reflecting functional divergence among its members [7.de Bello F. et al.Towards an assessment of multiple ecosystem processes and services via functional traits.Biodivers. Conserv. 2010; 19: 2873-2893Crossref Scopus (600) Google Scholar]. the ability of multiple, distinct organisms to perform a shared metabolic function [38.Allison S.D. Martiny J.B. Resistance, resilience, and redundancy in microbial communities.Proc. Natl. Acad. Sci. U. S. A. 2008; 105: 11512-11519Crossref PubMed Scopus (1525) Google Scholar]. Consequently, functional redundancy is often linked to functional stability against changing environments. the degree of change in an organism's or community’s functionality as a result of an environmental disturbance that may or may not be permanent over time [37.Doolittle W.F. Inkpen S.A. Processes and patterns of interaction as units of selection: An introduction to ITSNTS thinking.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: 4006-4014Crossref PubMed Scopus (38) Google Scholar]. the ability to return to the equilibrium state after a disturbance or not experience large changes in ecosystem functions across time [21.Talbot J.M. et al.Endemism and functional convergence across the North American soil mycobiome.Proc. Natl. Acad. Sci. U. S. A. 2014; 111: 6341-6346Crossref PubMed Scopus (335) Google Scholar,36.Goss-Souza D. et al.Amazon forest-to-agriculture conversion alters rhizosphere microbiome composition while functions are kept.FEMS Microbiol. Ecol. 2019; 95fiz009Crossref PubMed Scopus (16) Google Scholar,37.Doolittle W.F. Inkpen S.A. Processes and patterns of interaction as units of selection: An introduction to ITSNTS thinking.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: 4006-4014Crossref PubMed Scopus (38) Google Scholar]. Therefore, functional stability includes both functional resilience and resistance. any heritable characteristic that affects an organism's fitness, performance, or metabolic function [2.Violle C. et al.Let the concept of trait be functional!.Oikos. 2007; 116: 882-892Crossref Scopus (2483) Google Scholar]. acquisition of a new gene by DNA transfer from another organism [19.Philippot L. et al.The ecological coherence of high bacterial taxonomic ranks.Nat. Rev. Microbiol. 2010; 8: 523-529Crossref PubMed Scopus (382) Google Scholar]. the variability among living microorganisms. Microbial diversity includes taxonomic, phylogenetic, and functional diversity. Microbial diversity also includes α-, β-, and γ-diversity. Using functional traits as an example, microbial α-diversity is the number of functional traits (i.e., trait richness) in a microbial community, with or without weighted trait abundance. Microbial β-diversity is the comparison between two communities, measured as the difference between community composition. Microbial β-diversity is often measured on a normalized scale from zero to one. A high β-diversity index indicates a low level of similarity, while a low β-diversity index shows a high level of similarity. Microbial γ-diversity is a measure of the overall diversity for different ecosystems within a region, also known as geographic-scale diversity. a space with a particular set of resources and environmental conditions that individual organisms exploit [19.Philippot L. et al.The ecological coherence of high bacterial taxonomic ranks.Nat. Rev. Microbiol. 2010; 8: 523-529Crossref PubMed Scopus (382) Google Scholar]. a random event that can affect population and community dynamics in microbial ecology, like the flip of a coin. Those events include reproduction, mortality, dispersal, and disturbance involving random numbers in modeling [52.Hubbell S.P. 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