TY - JOUR
T1 - Natural bacterial assemblages in arabidopsis thaliana tissues become more distinguishable and diverse during host development
AU - Beilsmith, Kathleen
AU - Perisin, Matthew
AU - Bergelson, Joy
N1 - Funding Information:
K.B. and M.P. were supported by the University of Chicago Biological Sciences Division and by NIH T32 GM07197. M.P. was supported by a Department of Education GAANN grant in ecology to Cathy Pfister. Research was supported by NIH grant R01 GM083068 to J.B. Computing resources were provided by The Center for Research Informatics, funded by the Biological Sciences Division at the University of Chicago, with additional funding provided by the Institute for Translational Medicine, CTSA grant number UL1 TR000430, from the National Institutes of Health. We thank Dave Francis at the Michigan State Southwest Michigan Research and Extension Center for providing and prepping field plots. We thank Carlos Sahagun for assisting with planting and Timothy Morton, Benjamin Brachi, Talia Karasov, Manfred Ruddat, and Roderick Woolley for assistance with sampling. The DNA extraction and 16S amplicon sequencing protocols were developed in collaboration with Benjamin Brachi, and Alison Anastasio provided experimental design advice. Members of the Bergelson lab and the Department of Ecology and Evolution at the University of Chicago, in particular Caroline Oldstone-Jackson and Brooke Weigel, provided valuable feedback during the data processing and analysis. We thank two anonymous reviewers for their corrections and suggestions for the manuscript. M.P. and J.B. conceived and designed the study. M.P. executed the study and performed preliminary analysis. K.B. performed the data processing and analysis for the manuscript and wrote the manuscript with input from all authors. This work spanned the graduate training of the two first authors. M.P. led the field study, collected the data, and wrote the first analysis of the project in his dissertation. K.B. reanalyzed the data using a new bioinformatic pipeline and wrote the manuscript.
Funding Information:
K.B. and M.P. were supported by the University of Chicago Biological Sciences Division and by NIH T32 GM07197. M.P. was supported by a Department of Education GAANN grant in ecology to Cathy Pfister. Research was supported by NIH grant R01 GM083068 to J.B. Computing resources were provided by The Center for Research Informatics, funded by the Biological Sciences Division at the University of Chicago, with additional funding provided by the Institute for Translational Medicine, CTSA grant number UL1 TR000430, from the National Institutes of Health.
Publisher Copyright:
© 2021 Beilsmith et al.
PY - 2021/1/1
Y1 - 2021/1/1
N2 - To study the spatial and temporal dynamics of bacterial colonization under field conditions, we planted and sampled Arabidopsis thaliana during 2 years at two Michigan sites and surveyed colonists by sequencing 16S rRNA gene ampli-cons. Mosaic and dynamic assemblages revealed the plant as a patchwork of tissue habitats that differentiated with age. Although assemblages primarily varied between roots and shoots, amplicon sequence variants (ASVs) also differentiated phyllosphere tissues. Increasing assemblage diversity indicated that variants dispersed more widely over time, decreasing the importance of stochastic variation in early colonization relative to tissue differences. As tissues underwent developmental transitions, the root and phyllosphere assemblages became more distinct. This pattern was driven by common variants rather than those restricted to a particular tissue or transiently present at one developmental stage. Patterns also depended critically on fine phylogenetic resolution: when ASVs were grouped at coarse taxonomic levels, their associations with host tissue and age weakened. Thus, the observed spatial and temporal variation in colonization depended upon bacterial traits that were not broadly shared at the family level. Some colonists were consistently more successful at entering specific tissues, as evidenced by their repeatable spatial prevalence distributions across sites and years. However, these variants did not overtake plant assemblages, which instead became more even over time. Together, these results suggested that the increasing effect of tissue type was related to colonization bottlenecks for specific ASVs rather than to their ability to dominate other colonists once established. IMPORTANCE Developing synthetic microbial communities that can increase plant yield or deter pathogens requires basic research on several fronts, including the effi-ciency with which microbes colonize plant tissues, how plant genes shape the micro-biome, and the microbe-microbe interactions involved in community assembly. Findings on each of these fronts depend upon the spatial and temporal scales at which plant microbiomes are surveyed. In our study, phyllosphere tissues housed increasingly distinct microbial assemblages as plants aged, indicating that plants can be considered collections of tissue habitats in which microbial colonists—natural or synthetic—are established with differing success. Relationships between host genes and community diversity might vary depending on when samples are collected, given that assemblages grew more diverse as plants aged. Both spatial and temporal trends weakened when colonists were grouped by family, suggesting that functional rather than taxonomic profiling will be necessary to understand the basis for differences in colonization success.
AB - To study the spatial and temporal dynamics of bacterial colonization under field conditions, we planted and sampled Arabidopsis thaliana during 2 years at two Michigan sites and surveyed colonists by sequencing 16S rRNA gene ampli-cons. Mosaic and dynamic assemblages revealed the plant as a patchwork of tissue habitats that differentiated with age. Although assemblages primarily varied between roots and shoots, amplicon sequence variants (ASVs) also differentiated phyllosphere tissues. Increasing assemblage diversity indicated that variants dispersed more widely over time, decreasing the importance of stochastic variation in early colonization relative to tissue differences. As tissues underwent developmental transitions, the root and phyllosphere assemblages became more distinct. This pattern was driven by common variants rather than those restricted to a particular tissue or transiently present at one developmental stage. Patterns also depended critically on fine phylogenetic resolution: when ASVs were grouped at coarse taxonomic levels, their associations with host tissue and age weakened. Thus, the observed spatial and temporal variation in colonization depended upon bacterial traits that were not broadly shared at the family level. Some colonists were consistently more successful at entering specific tissues, as evidenced by their repeatable spatial prevalence distributions across sites and years. However, these variants did not overtake plant assemblages, which instead became more even over time. Together, these results suggested that the increasing effect of tissue type was related to colonization bottlenecks for specific ASVs rather than to their ability to dominate other colonists once established. IMPORTANCE Developing synthetic microbial communities that can increase plant yield or deter pathogens requires basic research on several fronts, including the effi-ciency with which microbes colonize plant tissues, how plant genes shape the micro-biome, and the microbe-microbe interactions involved in community assembly. Findings on each of these fronts depend upon the spatial and temporal scales at which plant microbiomes are surveyed. In our study, phyllosphere tissues housed increasingly distinct microbial assemblages as plants aged, indicating that plants can be considered collections of tissue habitats in which microbial colonists—natural or synthetic—are established with differing success. Relationships between host genes and community diversity might vary depending on when samples are collected, given that assemblages grew more diverse as plants aged. Both spatial and temporal trends weakened when colonists were grouped by family, suggesting that functional rather than taxonomic profiling will be necessary to understand the basis for differences in colonization success.
KW - 16S RNA
KW - Environmental microbiology
KW - Microbial communities
KW - Plant-microbe interactions
UR - http://www.scopus.com/inward/record.url?scp=85100075456&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85100075456&partnerID=8YFLogxK
U2 - 10.1128/mBio.02723-20
DO - 10.1128/mBio.02723-20
M3 - Article
C2 - 33468687
AN - SCOPUS:85100075456
VL - 12
SP - 1
EP - 16
JO - mBio
JF - mBio
SN - 2161-2129
IS - 1
M1 - e02723-20
ER -