Microdiversity shapes the traits, niche space, and biogeography of microbial taxa

Abstract

With rapidly improving sequencing technologies, scientists have recently gained the ability to examine diverse microbial communities at high genomic resolution, revealing that both free-living and host-associated microbes partition their environment at fine phylogenetic scales. This 'microdiversity,' or closely related (> 97% similar 16S rRNA gene) but ecologically and physiologically distinct sub-taxonomic groups, appears to be an intrinsic property of microorganisms. However, the functional implications of microdiversity as well as its effects on microbial biogeography are poorly understood. Here, we present two theoretical models outlining the evolutionary mechanisms that drive the formation of microdiverse 'sub-taxa.' Additionally, we review recent literature and reveal that microdiversity influences a wide range of functional traits across diverse ecosystems and microbes. Moving to higher levels of organization, we use laboratory data from marine, soil, and host-associated bacteria to demonstrate that the aggregated trait-based response of microdiverse sub-taxa modifies the fundamental niche of microbes. The correspondence between microdiversity and niche space represents a critical tool for future studies of microbial ecology. By combining growth experiments on diverse isolates with examinations of environmental abundance patterns, researchers can better quantify the fundamental and realized niches of microbes and improve understanding of microbial biogeography and response to future environmental change.

Microbial functional diversity: From concepts to applications

“…Ideally, fundamental and realized niches should be assessed simultaneously to determine whether observed differences in realized functions arise from different environmental conditions acting on a similar functional potential or from different potential between communities (Louca et al, ). For a recent review on the topic of ecological niches of microbes, the reader is invited to read the brilliant piece on microdiversity by Larkin and Martiny ().…”

Understanding How Microbiomes Influence The Systems They Inhabit: Moving From A Correlative To A Causal Research Framework

“…For example, the kinetics of a single metabolic pathway in a model 136 organism may help us understand the rate limiting steps of a narrow process, but 137 insights from model organisms are much less likely to capture the full spectrum of 138 responses of a broad process where phenotypic variation among phylogenetically 139 diverse organisms is likely to be much greater 15,16 . Defining the ecosystem process, 140 its critical sub-processes, and the known phylogenetic distribution of the metabolic 141 pathways that drive those sub-processes creates an explicit conceptual pathway that 142 links the ecosystem process to the microorganisms that contribute to it.…”

“…demonstrated immense variation within a given OTU (i.e., "microdiversity") that in 367 part explains the challenge of linking membership to a community property 16 . For 368 example, work on Prochlorococcus has led to a better understanding of how 369 ecotypes within a single taxonomic unit (OTU) can lead to specialization in 370 temperature and substrate affinity 41 .…”

“…For 368 example, work on Prochlorococcus has led to a better understanding of how 369 ecotypes within a single taxonomic unit (OTU) can lead to specialization in 370 temperature and substrate affinity 41 . OTUs that form a substantial portion of the 371 microbiome's sequence abundance provide potential candidates for further 372 investigation of possible phenotypic plasticity and or microdiversity 16 . For example, a 373 single phylotype of the class Spartobacteria within the phyla Verrucomicrobia was 374 21, 2016; found to be present in a broad range of soil ecosystems and comprised as much as 375 31% of all 16S sequences returned from prairie soils 42 , making it an excellent 376 candidate for targeted isolation and physiological studies.…”

On the development of a predictive functional trait approach for studying terrestrial arthropods

“…While the functional trait approach has an important history in plant ecology (Cadotte et al., ; Cornelissen et al., ; Wright et al., ), there has been an increasing interest to adapt the approach to study animals (Luck, Lavorel, McIntyre, & Lumb, ; Moretti et al., ; Pey, Nahmani et al., ) and microbes (Larkin & Martiny, ), so as to improve our understanding of multitrophic interactions (de Bello et al., ; Gravel, Albouy, & Thuiller, ; Lavorel et al., ). Although in theory, very broad trait axes (or economic spectra) reflecting resource acquisition, growth, dispersal, etc., are common to all organisms (Litchman, Ohman, & Kiørboe, ; Salguero‐Gómez et al., ), moving beyond plants requires defining new types of traits.…”