Soil microbial growth rate, trophic strategy, and the oligotroph–copiotroph continuum
Chansotheary Dang, Juan Piñeiro Nevado, Ronald Schartiger, Binu M. Tripathi, Jeth G. Walkup, Edward Brzostek, Ember M. MorrisseyABSTRACT
The oligotroph–copiotroph continuum is an ecological framework that describes microbial metabolic traits, habitat preferences, and growth strategies. As microbial growth rates determine soil element cycling, understanding microbial trophic strategies is critical for improving predictions of ecosystem biogeochemistry. However, accurately determining microbial trophic strategies has been challenging for soil microorganisms. Here, we examined microbial growth rates (via 18 O-quantitative stable isotope probing) in rhizosphere and bulk forest soils and proposed a new approach to determine the trophic strategies of microbial taxa. Growth rates were log-normally distributed and used to classify 35% of bacterial taxa as oligotrophs (lowest growth rates), 50% as mesotrophs (intermediate growth rates), and 15% as copiotrophs (highest growth rates). The average growth rates of individual taxa exhibited phylogenetic organization, suggesting that growth rates are constrained by vertically transmitted genomic traits under varying conditions. Consistent with the expected habitat preferences, copiotrophs were more abundant and active in the rhizosphere, while bulk soil was dominated by slow-growing oligotrophs. Carbon addition positively impacted copiotroph growth rates in both the rhizosphere and bulk soil. Oligotrophic and mesotrophic taxa benefited from carbon addition in the bulk soil, but not in the rhizosphere, perhaps due to intensified competition with a large population of copiotrophs. Taken together, these results demonstrate that microbial growth rates are tied to bacterial habitat preferences and carbon responses, suggesting they may be strong indicators of trophic strategy.
IMPORTANCE
Despite compelling culture-based evidence for the oligotroph–copiotroph framework, scientists have struggled for decades to meaningfully characterize the trophic strategies of soil microorganisms, perhaps due to methodological limitations. This work uses a growth rate approach to determine the trophic strategies of microbial taxa that is validated by testing two classic hypotheses regarding microbial trophic strategy in soil. The results support the use of growth rate–based trophic strategy classification and demonstrate that microbial growth rates are constrained by evolutionary history such that fine (e.g., families and genera) but not coarse (e.g., phyla and orders) taxonomic groups may be meaningfully described as oligotrophs or copiotrophs. These results are of broad relevance, as they suggest that growth rate measurements may be used to make a prevailing ecological theory describing all unicellular microbial life on Earth (i.e., the oligotroph–copiotroph framework) more quantitative and robust.