Abstract
Temporal variation in community composition is central to our understanding of the assembly and functioning of microbial communities, yet the controls over temporal dynamics for microbiomes of long-lived plants, such as trees, remain unclear. Temporal variation in tree microbiomes could arise primarily from seasonal (i.e., intra-annual) fluctuations in community composition or from longer-term changes across years as host plants age. To test these alternatives, we experimentally isolated temporal variation in plant microbiome composition using a common garden and clonally propagated plants, and we used amplicon sequencing to characterize bacterial/archaeal and fungal communities in the leaf endosphere, root endosphere, and rhizosphere of two Populus spp. over four seasons across two consecutive years. Microbial community composition differed among seasons and years (which accounted for up to 21% of the variation in microbial community composition) and was correlated with seasonal dissimilarity in climatic conditions. However, microbial community dissimilarity was also positively correlated with time, reflecting longer-term compositional shifts as host trees aged. Together, our findings demonstrate that temporal patterns in tree microbiomes arise from both seasonal fluctuations and longer-term changes, which interact to generate unique seasonal patterns each year. In addition to shedding light on two important controls over the assembly of plant microbiomes, our results also suggest future studies of tree microbiomes should account for background temporal dynamics when testing the drivers of spatial patterns in microbial community composition and temporal responses of plant microbiomes to environmental change.
| Original language | English |
|---|---|
| Journal | mSystems |
| Volume | 9 |
| Issue number | 3 |
| DOIs | |
| State | Published - Mar 2024 |
Funding
We thank Michele Thornton and Bruce Wilson for guidance on accessing DAYMET daily surface weather data. We are grateful for insightful comments from Dale Pelletier on an earlier version of this article. We also thank the University of Tennessee Institute of Agriculture—East Tennessee AgResearch and Education Center for providing the site access and for allowing us to establish a plantation at their field site and assisting in its maintenance. We also thank two anonymous reviewers for their thoughtful and constructive feedback on a previous version of this article. This research was sponsored by the Genomic Science Program, United States Department of Energy, Office of Science, Biological and Environmental Research, as part of the Plant-Microbe Interfaces Science Focus Area at Oak Ridge National Laboratory (ORNL). ORNL is managed by UT-Battelle, LLC, for the United States Department of Energy under contract DEAC05-00OR22725. M.A.C., C.W.S., and W.M. designed the study and set up the common garden experiment. M.A.C., C.W.S., N.C.D., A.M.V., and A.A.C. conducted the field work. A.A.C., D.M.K., N.C.D., K.P., A.B.W., and W.A.A. performed the laboratory analyses. W.A.A. analyzed the data and wrote the first draft of the article. All authors contributed to article revisions. This research was sponsored by the Genomic Science Program, United States Department of Energy, of Science, Biological and Environmental Research, as part of the Plant-Microbe Interfaces Science Focus Area at Oak Ridge National Laboratory (ORNL). ORNL is managed by UT-Battelle, LLC, for the United States Department of Energy under contract DEAC05-00OR22725.
Keywords
- fine roots
- microbial community assembly
- phyllosphere
- rhizosphere
- temporal patterns