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Synergistic Cues from Diverse Bacteria Enhance Multicellular Development in a Choanoflagellate

Bacteria regulate the life histories of diverse eukaryotes, but relatively little is known about how eukaryotes interpret and respond to multiple bacterial cues encountered simultaneously. To explore how a eukaryote might respond to a combination of bioactive molecules from multiple bacteria, we tre...

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Detalles Bibliográficos
Autores principales: Ireland, Ella V., Woznica, Arielle, King, Nicole
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7237790/
https://www.ncbi.nlm.nih.gov/pubmed/32220848
http://dx.doi.org/10.1128/AEM.02920-19
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author Ireland, Ella V.
Woznica, Arielle
King, Nicole
author_facet Ireland, Ella V.
Woznica, Arielle
King, Nicole
author_sort Ireland, Ella V.
collection PubMed
description Bacteria regulate the life histories of diverse eukaryotes, but relatively little is known about how eukaryotes interpret and respond to multiple bacterial cues encountered simultaneously. To explore how a eukaryote might respond to a combination of bioactive molecules from multiple bacteria, we treated the choanoflagellate Salpingoeca rosetta with two sets of bacterial cues, one that induces mating and another that induces multicellular development. We found that simultaneous exposure to both sets of cues enhanced multicellular development in S. rosetta, eliciting both larger multicellular colonies and an increase in the number of colonies. Thus, rather than conveying conflicting sets of information, these distinct bacterial cues synergize to augment multicellular development. This study demonstrates how a eukaryote can integrate and modulate its response to cues from diverse bacteria, underscoring the potential impact of complex microbial communities on eukaryotic life histories. IMPORTANCE Eukaryotic biology is profoundly influenced by interactions with diverse environmental and host-associated bacteria. However, it is not well understood how eukaryotes interpret multiple bacterial cues encountered simultaneously. This question has been challenging to address because of the complexity of many eukaryotic model systems and their associated bacterial communities. Here, we studied a close relative of animals, the choanoflagellate Salpingoeca rosetta, to explore how eukaryotes respond to diverse bacterial cues. We found that a bacterial chondroitinase that induces mating on its own can also synergize with bacterial lipids that induce multicellular “rosette” development. When encountered together, these cues enhance rosette development, resulting in both the formation of larger rosettes and an increase in the number of rosettes compared to rosette development in the absence of the chondroitinase. These findings highlight how synergistic interactions among bacterial cues can influence the biology of eukaryotes.
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spelling pubmed-72377902020-06-09 Synergistic Cues from Diverse Bacteria Enhance Multicellular Development in a Choanoflagellate Ireland, Ella V. Woznica, Arielle King, Nicole Appl Environ Microbiol Microbial Ecology Bacteria regulate the life histories of diverse eukaryotes, but relatively little is known about how eukaryotes interpret and respond to multiple bacterial cues encountered simultaneously. To explore how a eukaryote might respond to a combination of bioactive molecules from multiple bacteria, we treated the choanoflagellate Salpingoeca rosetta with two sets of bacterial cues, one that induces mating and another that induces multicellular development. We found that simultaneous exposure to both sets of cues enhanced multicellular development in S. rosetta, eliciting both larger multicellular colonies and an increase in the number of colonies. Thus, rather than conveying conflicting sets of information, these distinct bacterial cues synergize to augment multicellular development. This study demonstrates how a eukaryote can integrate and modulate its response to cues from diverse bacteria, underscoring the potential impact of complex microbial communities on eukaryotic life histories. IMPORTANCE Eukaryotic biology is profoundly influenced by interactions with diverse environmental and host-associated bacteria. However, it is not well understood how eukaryotes interpret multiple bacterial cues encountered simultaneously. This question has been challenging to address because of the complexity of many eukaryotic model systems and their associated bacterial communities. Here, we studied a close relative of animals, the choanoflagellate Salpingoeca rosetta, to explore how eukaryotes respond to diverse bacterial cues. We found that a bacterial chondroitinase that induces mating on its own can also synergize with bacterial lipids that induce multicellular “rosette” development. When encountered together, these cues enhance rosette development, resulting in both the formation of larger rosettes and an increase in the number of rosettes compared to rosette development in the absence of the chondroitinase. These findings highlight how synergistic interactions among bacterial cues can influence the biology of eukaryotes. American Society for Microbiology 2020-05-19 /pmc/articles/PMC7237790/ /pubmed/32220848 http://dx.doi.org/10.1128/AEM.02920-19 Text en Copyright © 2020 Ireland et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Microbial Ecology
Ireland, Ella V.
Woznica, Arielle
King, Nicole
Synergistic Cues from Diverse Bacteria Enhance Multicellular Development in a Choanoflagellate
title Synergistic Cues from Diverse Bacteria Enhance Multicellular Development in a Choanoflagellate
title_full Synergistic Cues from Diverse Bacteria Enhance Multicellular Development in a Choanoflagellate
title_fullStr Synergistic Cues from Diverse Bacteria Enhance Multicellular Development in a Choanoflagellate
title_full_unstemmed Synergistic Cues from Diverse Bacteria Enhance Multicellular Development in a Choanoflagellate
title_short Synergistic Cues from Diverse Bacteria Enhance Multicellular Development in a Choanoflagellate
title_sort synergistic cues from diverse bacteria enhance multicellular development in a choanoflagellate
topic Microbial Ecology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7237790/
https://www.ncbi.nlm.nih.gov/pubmed/32220848
http://dx.doi.org/10.1128/AEM.02920-19
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