A new perspective on functional redundancy and phylogenetic niche conservatism in soil microbial communities

Abstract

Functional redundancy in soil microbial communities seems to contradict the notion that individual species have distinct metabolic niches in multi-species communities. All soil microbiota have the metabolic capacity for “basic” functions (e.g., respiration and nitrogen and phosphorus cycling), but only a few soil microbiota participate in “rare” functions (e.g., methanogenesis and mineralization of recalcitrant organic pollutants). The objective of this perspective paper is to use the phylogenetic niche conservatism theory as an explanation for the functional redundancy of soil microbiota. Phylogenetic niche conservatism is defined as the tendency for lineages to retain ancestral functional characteristics through evolutionary time-scales. The present-day soil microbiota is the result of a community assembly process that started when prokaryotes first appeared on Earth. For billions of years, microbiota have retained a highly conserved set of core genes that control the essential redox and biogeochemical reactions for life on Earth. These genes are passed from microbe to microbe, which contributes to functional redundancy in soil microbiota at the planetary scale. The assembly of microbial communities during soil formation is consistent with phylogenetic niche conservatism. Within a specific soil, the heterogeneous matrix provides an infinite number of sets of diverse environmental conditions, i.e., niches that lead to the divergence of microbial species. The phylogenetic niche conservatism theory predicts that two or more microbial species diverging from the same clade will have an overlap in their niches, implying that they are functionally redundant in some of their metabolic processes. The endogenous genetic factors that constrain the adaptation of individuals and, thus, populations to changing environmental conditions constitute the core process of phylogenetic niche conservatism. Furthermore, the degree of functional redundancy in a particular soil is proportional to the complexity of the considered function. We conclude with a conceptual model that identifies six patterns of functional redundancy in soil microbial communities, consistent with the phylogenetic niche conservatism theory.