Linking Microbial Community Structure to Trait Distributions and Functions Using Salinity as an Environmental Filter

Abstract

The structure and function of microbial communities vary along environmental gradients; however, interlinking the two has been challenging. In this study, salinity was used as an environmental filter to study how it could shape trait distributions, community structures, and the resulting functions of soil microbes. The environmental filter was applied by salinizing nonsaline soil (0 to 22 mg NaCl g−1). Our targeted community trait distribution (salt tolerance) was determined with dose-response relationships between bacterial growth and salinity. The bacterial community structure responses were resolved with Illumina 16S rRNA gene amplicon sequencing, and the microbial functions determined were respiration and bacterial and fungal growth. Salt exposure quickly resulted in filtered trait distributions, and stronger filters resulted in larger shifts. The filtered trait distributions correlated well with community composition differences, suggesting that trait distribution shifts were driven at least partly by species turnover. While salt exposure decreased respiration, microbial growth responses appeared to be characterized by competitive interactions. Fungal growth was highest when bacterial growth was inhibited by the highest salinity, and it was lowest when the bacterial growth rate peaked at intermediate salt levels. These findings corroborated a higher potential for fungal salt tolerance than bacterial salt tolerance for communities derived from a nonsaline soil. In conclusion, by using salt as an environmental filter, we could interlink the targeted trait distribution with both the community structure and resulting functions of soil microbes. IMPORTANCE Understanding the role of ecological communities in maintaining multiple ecosystem processes is a central challenge in ecology. Soil microbial communities perform vital ecosystem functions, such as the decomposition of organic matter to provide plant nutrition. However, despite the functional importance of soil microorganisms, attribution of ecosystem function to particular constituents of the microbial community has been impeded by a lack of information linking microbial processes to community composition and structure. Here, we apply a conceptual framework to determine how microbial communities influence ecosystem processes, by applying a “top-down” trait-based approach. By determining the dependence of microbial processes on environmental factors (e.g., the tolerance to salinity), we can define the aggregate response trait distribution of the community, which then can be linked to the community structure and the resulting function performed by the microbial community.

Shifts in the soil bacterial community along a salinity gradient in the Yellow River Delta

“…Salinity has been reported to selectively affect certain phylogenetic groups by markedly reducing cell-specific activities and growth efficiency (Del Giorgio & Bouvier, 2002). Simultaneously, microbes physiologically adapt to offset the adverse effects of salinity (Rath, Maheshwari, Rousk, & Bailey, 2019). Therefore, the changing salinity could act as an environmental filter for bacterial community, possibly leading to the 'loss' or the 'activation' of some species (Rath et al, 2019).…”

“…Simultaneously, microbes physiologically adapt to offset the adverse effects of salinity (Rath, Maheshwari, Rousk, & Bailey, 2019). Therefore, the changing salinity could act as an environmental filter for bacterial community, possibly leading to the 'loss' or the 'activation' of some species (Rath et al, 2019). Salinity has been confirmed to directly affect the bacterial community in different ways.…”

Effects of forced taxonomic transitions on metabolic composition and function in microbial microcosms

“…Another potential cause for the increased rate similarity could be that in the long term the fluxes in this A B C D poorly mixed system are strongly constrained by boundary conditions and physical transport properties (Louca et al, 2019). A negative effect of salinity on metabolic rates has been observed previously, especially when microorganisms were originally taken from a less saline environment (as in our case) (Wilson et al, 2013;Rath and Rousk, 2015;Peng et al, 2017;Navada et al, 2019;Rath et al, 2019). The effects of salinity are at least partly physiological in nature, with salinity imposing a stress to cells (Rath and Rousk, 2015) that might lead to lower microbial population sizes and generally lower bulk metabolic rates.…”

“…Experiments with microcosms have been particularly useful for disentangling the relationships between environmental conditions, taxonomy, metabolic composition and metabolic function in microbial systems (Widder et al, 2016). Many experiments use chemical treatments to modify microbial taxonomic composition in microcosms, and then examine the effects on a given function (Girvan et al, 2005;Langenheder et al, 2005Langenheder et al, , 2006Peter et al, 2011;Harter et al, 2014;Peng et al, 2017;Rath et al, 2019). Common garden experiments, where microbial communities of different origins are subjected to identical conditions, have also been used to examine the potential effects of origin on metabolic rates (Strickland et al, 2009;Reed and Martiny, 2013;Martiny et al, 2017).…”

Mobile microbiome networks across spatiotemporal gradients

“…Increasing evidence shows that microbial community composition changes along environmental gradients [12,13] and from healthy to diseased states [4,14]. Most existing approaches can only infer a single aggregate network from a number of samples, failing to characterize how microbial interactions vary according to geographic, biotic, and developmental contexts and further chart causal links between these interactions and biogeochemical cycling or host phenotypes.…”