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

Abstract

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 experimental chemostats and trait-based modeling, we examine how the composition of a microbial community collected from a coastal meromictic pond changes as dilution rate increases from 0.1 to 10 d-1. We compare 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 is initially evenly distributed across the community and another where maximum specific growth rate traits are pulled from a beta probability distribution that is skewed towards low specific growth rates. Our experimental results match the simulation where the initial natural population is dominated by slow-growing microbes. Our results also highlight 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 temperature or pH. An organisms maximum specific growth rate places a lower bound on the residence or turnover time of a system where an organism can persist without being removed from the system. While we have good bounds on the maximum specific growth rate of culturable organisms, 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. Using chemostats and trait-based modeling, this study assesses how maximum specific growth rate is distributed in a natural community collected from a coastal, salinity-stratified pond.