What taxon-specific growth measurements reveal about microbial growth strategies in natural soil communities

Heterotrophic microorganisms decompose soil organic matter to assimilate organic compounds that provide energy and carbon for growth and maintenance. The growth of microbial communities is thus at the heart of the carbon cycle, and understanding how microbial growth is controlled is arguably of paramount importance for understanding global carbon cycling in the present and future climate.  Most information on microbial growth comes from work with pure cultures (population level) or from studies of microbial community growth, while understanding the growth of individual microbial taxa in natural communities is poorly studied and understood. However, with the advent of new stable isotope probing techniques based on 18O from labelled water, it is now possible to look beyond the community level to the growth of individual populations of microorganisms in complex soil communities. In addition, recent advances in labelling growing microbial taxa without the addition of liquid water, the so-called ‘vapor qSIP', allow us to analyze microbial growth in complex communities without changing environmental conditions, a prerequisite for studying the behavior of microbial communities in climate change experiments. We report here on two climate change experiments in which we performed taxon-resolved growth measurements under different environmental conditions. Our results show the following: (1) Contrary to our expectations, changing environmental conditions (e.g., soil warming and drought) led to a change in the number of actively growing bacterial taxa, but not in their growth rates. Among other things, this challenges the paradigm developed from a plethora of measurements of microbial community growth that microbial physiology is accelerated by higher temperatures. (2) Many microbial taxa were only actively dividing in specific climate change treatments, i.e., under specific environmental conditions. We conclude that the realized ecological niche of bacteria appears to be much smaller than community growth measurements suggest. Testing, for example, the temperature niche of individual populations (with presumably different functional traits) may therefore lead to very different predictions of soil functions in a future climate. (3) Compared to estimates of total soil microbial community composition (e.g., amplicon sequencing of the 16S rRNA gene), the actively growing community is more sensitive to changes in environmental conditions, allowing a more accurate prediction of community structure in a future climate and its functional roles in biogeochemistry. Overall, measuring taxon-resolved population growth rates of complex communities provides a novel, more nuanced and sophisticated picture of soil ecosystems, which may help to develop better predictions of structural and functional changes in microbial ecosystems in a future climate.