TY - JOUR
T1 - Conspecific versus heterospecific transmission shapes host specialization of the phyllosphere microbiome
AU - Meyer, Kyle M.
AU - Muscettola, Isabella E.
AU - Vasconcelos, Ana Luisa S.
AU - Sherman, Julia K.
AU - Metcalf, C. Jessica E.
AU - Lindow, Steven E.
AU - Koskella, Britt
N1 - Publisher Copyright: © 2023 The Authors
PY - 2023/12/13
Y1 - 2023/12/13
N2 - In disease ecology, pathogen transmission among conspecific versus heterospecific hosts is known to shape pathogen specialization and virulence, but we do not yet know if similar effects occur at the microbiome level. We tested this idea by experimentally passaging leaf-associated microbiomes either within conspecific or across heterospecific plant hosts. Although conspecific transmission results in persistent host-filtering effects and more within-microbiome network connections, heterospecific transmission results in weaker host-filtering effects but higher levels of interconnectivity. When transplanted onto novel plants, heterospecific lines are less differentiated by host species than conspecific lines, suggesting a shift toward microbiome generalism. Finally, conspecific lines from tomato exhibit a competitive advantage on tomato hosts against those passaged on bean or pepper, suggesting microbiome-level host specialization. Overall, we find that transmission mode and previous host history shape microbiome diversity, with repeated conspecific transmission driving microbiome specialization and repeated heterospecific transmission promoting microbiome generalism.
AB - In disease ecology, pathogen transmission among conspecific versus heterospecific hosts is known to shape pathogen specialization and virulence, but we do not yet know if similar effects occur at the microbiome level. We tested this idea by experimentally passaging leaf-associated microbiomes either within conspecific or across heterospecific plant hosts. Although conspecific transmission results in persistent host-filtering effects and more within-microbiome network connections, heterospecific transmission results in weaker host-filtering effects but higher levels of interconnectivity. When transplanted onto novel plants, heterospecific lines are less differentiated by host species than conspecific lines, suggesting a shift toward microbiome generalism. Finally, conspecific lines from tomato exhibit a competitive advantage on tomato hosts against those passaged on bean or pepper, suggesting microbiome-level host specialization. Overall, we find that transmission mode and previous host history shape microbiome diversity, with repeated conspecific transmission driving microbiome specialization and repeated heterospecific transmission promoting microbiome generalism.
KW - community coalescence
KW - experimental evolution
KW - microbiome assembly
KW - microbiome engineering
KW - microbiome generalism
KW - microbiome passaging
KW - microbiome specialization
KW - microbiome transmission
KW - phyllosphere
UR - http://www.scopus.com/inward/record.url?scp=85179131440&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85179131440&partnerID=8YFLogxK
U2 - 10.1016/j.chom.2023.11.002
DO - 10.1016/j.chom.2023.11.002
M3 - Article
C2 - 38029741
SN - 1931-3128
VL - 31
SP - 2067-2079.e5
JO - Cell Host and Microbe
JF - Cell Host and Microbe
IS - 12
ER -