Interspecific interactions facilitate keystone species in a multispecies biofilm that promotes plant growth
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Interspecific interactions facilitate keystone species in a multispecies biofilm that promotes plant growth. / Yang, Nan; Røder, Henriette L.; Wicaksono, Wisnu Adi; Wassermann, Birgit; Russel, Jakob; Li, Xuanji; Nesme, Joseph; Berg, Gabriele; Sørensen, Søren J.; Burmølle, Mette.
In: The ISME Journal, Vol. 18, No. 1, 2024.Research output: Contribution to journal › Journal article › Research › peer-review
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TY - JOUR
T1 - Interspecific interactions facilitate keystone species in a multispecies biofilm that promotes plant growth
AU - Yang, Nan
AU - Røder, Henriette L.
AU - Wicaksono, Wisnu Adi
AU - Wassermann, Birgit
AU - Russel, Jakob
AU - Li, Xuanji
AU - Nesme, Joseph
AU - Berg, Gabriele
AU - Sørensen, Søren J.
AU - Burmølle, Mette
N1 - Publisher Copyright: © The Author(s) 2024. Published by Oxford University Press on behalf of the International Society for Microbial Ecology.
PY - 2024
Y1 - 2024
N2 - Microorganisms colonizing plant roots co-exist in complex, spatially structured multispecies biofilm communities. However, little is known about microbial interactions and the underlying spatial organization within biofilm communities established on plant roots. Here, a well-established four-species biofilm model (Stenotrophomonas rhizophila, Paenibacillus amylolyticus, Microbacterium oxydans, and Xanthomonas retroflexus, termed as SPMX) was applied to Arabidopsis roots to study the impact of multispecies biofilm on plant growth and the community spatial dynamics on the roots. SPMX co-culture notably promoted root development and plant biomass. Co-cultured SPMX increased root colonization and formed multispecies biofilms, structurally different from those formed by monocultures. By combining 16S rRNA gene amplicon sequencing and fluorescence in situ hybridization with confocal laser scanning microscopy, we found that the composition and spatial organization of the four-species biofilm significantly changed over time. Monoculture P. amylolyticus colonized plant roots poorly, but its population and root colonization were highly enhanced when residing in the four-species biofilm. Exclusion of P. amylolyticus from the community reduced overall biofilm production and root colonization of the three species, resulting in the loss of the plant growth-promoting effects. Combined with spatial analysis, this led to identification of P. amylolyticus as a keystone species. Our findings highlight that weak root colonizers may benefit from mutualistic interactions in complex communities and hereby become important keystone species impacting community spatial organization and function. This work expands the knowledge on spatial organization uncovering interspecific interactions in multispecies biofilm communities on plant roots, beneficial for harnessing microbial mutualism promoting plant growth.
AB - Microorganisms colonizing plant roots co-exist in complex, spatially structured multispecies biofilm communities. However, little is known about microbial interactions and the underlying spatial organization within biofilm communities established on plant roots. Here, a well-established four-species biofilm model (Stenotrophomonas rhizophila, Paenibacillus amylolyticus, Microbacterium oxydans, and Xanthomonas retroflexus, termed as SPMX) was applied to Arabidopsis roots to study the impact of multispecies biofilm on plant growth and the community spatial dynamics on the roots. SPMX co-culture notably promoted root development and plant biomass. Co-cultured SPMX increased root colonization and formed multispecies biofilms, structurally different from those formed by monocultures. By combining 16S rRNA gene amplicon sequencing and fluorescence in situ hybridization with confocal laser scanning microscopy, we found that the composition and spatial organization of the four-species biofilm significantly changed over time. Monoculture P. amylolyticus colonized plant roots poorly, but its population and root colonization were highly enhanced when residing in the four-species biofilm. Exclusion of P. amylolyticus from the community reduced overall biofilm production and root colonization of the three species, resulting in the loss of the plant growth-promoting effects. Combined with spatial analysis, this led to identification of P. amylolyticus as a keystone species. Our findings highlight that weak root colonizers may benefit from mutualistic interactions in complex communities and hereby become important keystone species impacting community spatial organization and function. This work expands the knowledge on spatial organization uncovering interspecific interactions in multispecies biofilm communities on plant roots, beneficial for harnessing microbial mutualism promoting plant growth.
KW - interspecies interactions
KW - keystone species
KW - multispecies biofilms
KW - mutualism
KW - plant growth
KW - spatial organization
U2 - 10.1093/ismejo/wrae012
DO - 10.1093/ismejo/wrae012
M3 - Journal article
C2 - 38365935
AN - SCOPUS:85187786152
VL - 18
JO - I S M E Journal
JF - I S M E Journal
SN - 1751-7362
IS - 1
ER -
ID: 386377217