Growth characteristics of natural microbial populations are skewed toward bacteria with low specific growth rates

Microbes are often functionally characterized by traits that specify their optimum environmental conditions for growth, such as temperature or pH, as well as upper and lower bounds where growth is possible. While any given microbe will have a narrow environmental window where growth can occur, a diverse community can span a much larger range of conditions where growth is possible by at least some members of the community. One important trait of microbes is maximum specific growth rate, as this trait determines if a microbe can persist in environments with short residence times. In this study, we conducted a chemostat experiment with natural microbial communities and manipulated dilution rate to test how it would act as a selective force controlling community dynamics and microbial diversity. Using both the experimental chemostats, as well as trait-based modeling, we examined how the composition of a microbial community collected from a coastal meromictic pond changed as dilution rate increased from 0.1 to 10 day^-1. We compared experimental results from 16S rRNA gene amplicon sequences to the output from two different simulations of the trait-based model, one in which maximum specific growth rate was initially evenly distributed across the community, and another where maximum specific growth rate traits were pulled from a beta probability distribution that was skewed toward low specific growth rates. Experimental results matched the simulation where the initial natural population was dominated by slow-growing microbes, highlighting the importance of initial trait distributions in modeling community response to environmental changes.IMPORTANCEAll living organisms are constrained by environmental boundaries that govern where growth is possible, such as minimum and maximum temperatures or pH. An organism's maximum specific growth rate places a lower bound on the residence or turnover time where an organism can persist without being removed from the system. While there are laboratory constraints on the maximum specific growth rate of culturable microorganisms, such as Escherichia or Vibrio species, information is lacking on how the maximum specific growth rate trait is distributed in natural microbial communities. This information is critical for understanding how a community will respond to changes in residence time or other environmental perturbations. Using chemostats and trait-based modeling, this study assessed how maximum specific growth rate is distributed in a natural community collected from a coastal, salinity-stratified pond.