Bacterial alkylquinolone signaling contributes to structuring microbial communities in the ocean

Abstract Background Marine bacteria form complex relationships with eukaryotic hosts, from obligate symbioses to pathogenic interactions. These interactions can be tightly regulated by bioactive molecules, creating a complex system of chemical interactions through which these species chemically comm...

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Main Authors: Kristen E. Whalen, Jamie W. Becker, Anna M. Schrecengost, Yongjie Gao, Nicole Giannetti, Elizabeth L. Harvey
Format: Article
Language:English
Published: BMC 2019-06-01
Series:Microbiome
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40168-019-0711-9
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spelling doaj-20a26059bbf64463921fe96acca7d3f32020-11-25T02:24:59ZengBMCMicrobiome2049-26182019-06-017111710.1186/s40168-019-0711-9Bacterial alkylquinolone signaling contributes to structuring microbial communities in the oceanKristen E. Whalen0Jamie W. Becker1Anna M. Schrecengost2Yongjie Gao3Nicole Giannetti4Elizabeth L. Harvey5Department of Biology, Haverford CollegeDepartment of Biology, Haverford CollegeDepartment of Biology, Haverford CollegeDepartment of Biology, Haverford CollegeDepartment of Biology, Haverford CollegeSkidaway Institute of Oceanography, University of GeorgiaAbstract Background Marine bacteria form complex relationships with eukaryotic hosts, from obligate symbioses to pathogenic interactions. These interactions can be tightly regulated by bioactive molecules, creating a complex system of chemical interactions through which these species chemically communicate thereby directly altering the host’s physiology and community composition. Quorum sensing (QS) signals were first described in a marine bacterium four decades ago, and since then, we have come to discover that QS mediates processes within the marine carbon cycle, affects the health of coral reef ecosystems, and shapes microbial diversity and bacteria-eukaryotic host relationships. Yet, only recently have alkylquinolone signals been recognized for their role in cell-to-cell communication and the orchestration of virulence in biomedically relevant pathogens. The alkylquinolone, 2-heptyl-4-quinolone (HHQ), was recently found to arrest cell growth without inducing cell mortality in selected phytoplankton species at nanomolar concentrations, suggesting QS molecules like HHQ can influence algal physiology, playing pivotal roles in structuring larger ecological frameworks. Results To understand how natural communities of phytoplankton and bacteria respond to HHQ, field-based incubation experiments with ecologically relevant concentrations of HHQ were conducted over the course of a stimulated phytoplankton bloom. Bulk flow cytometry measurements indicated that, in general, exposure to HHQ caused nanoplankton and prokaryotic cell abundances to decrease. Amplicon sequencing revealed HHQ exposure altered the composition of particle-associated and free-living microbiota, favoring the relative expansion of both gamma- and alpha-proteobacteria, and a concurrent decrease in Bacteroidetes. Specifically, Pseudoalteromonas spp., known to produce HHQ, increased in relative abundance following HHQ exposure. A search of representative bacterial genomes from genera that increased in relative abundance when exposed to HHQ revealed that they all have the genetic potential to bind HHQ. Conclusions This work demonstrates HHQ has the capacity to influence microbial community organization, suggesting alkylquinolones have functions beyond bacterial communication and are pivotal in driving microbial community structure and phytoplankton growth. Knowledge of how bacterial signals alter marine communities will serve to deepen our understanding of the impact these chemical interactions have on a global scale.http://link.springer.com/article/10.1186/s40168-019-0711-9Quorum sensing2-heptyl-4-quinoloneMicrobiomePhytoplanktonPseudoalteromonas
collection DOAJ
language English
format Article
sources DOAJ
author Kristen E. Whalen
Jamie W. Becker
Anna M. Schrecengost
Yongjie Gao
Nicole Giannetti
Elizabeth L. Harvey
spellingShingle Kristen E. Whalen
Jamie W. Becker
Anna M. Schrecengost
Yongjie Gao
Nicole Giannetti
Elizabeth L. Harvey
Bacterial alkylquinolone signaling contributes to structuring microbial communities in the ocean
Microbiome
Quorum sensing
2-heptyl-4-quinolone
Microbiome
Phytoplankton
Pseudoalteromonas
author_facet Kristen E. Whalen
Jamie W. Becker
Anna M. Schrecengost
Yongjie Gao
Nicole Giannetti
Elizabeth L. Harvey
author_sort Kristen E. Whalen
title Bacterial alkylquinolone signaling contributes to structuring microbial communities in the ocean
title_short Bacterial alkylquinolone signaling contributes to structuring microbial communities in the ocean
title_full Bacterial alkylquinolone signaling contributes to structuring microbial communities in the ocean
title_fullStr Bacterial alkylquinolone signaling contributes to structuring microbial communities in the ocean
title_full_unstemmed Bacterial alkylquinolone signaling contributes to structuring microbial communities in the ocean
title_sort bacterial alkylquinolone signaling contributes to structuring microbial communities in the ocean
publisher BMC
series Microbiome
issn 2049-2618
publishDate 2019-06-01
description Abstract Background Marine bacteria form complex relationships with eukaryotic hosts, from obligate symbioses to pathogenic interactions. These interactions can be tightly regulated by bioactive molecules, creating a complex system of chemical interactions through which these species chemically communicate thereby directly altering the host’s physiology and community composition. Quorum sensing (QS) signals were first described in a marine bacterium four decades ago, and since then, we have come to discover that QS mediates processes within the marine carbon cycle, affects the health of coral reef ecosystems, and shapes microbial diversity and bacteria-eukaryotic host relationships. Yet, only recently have alkylquinolone signals been recognized for their role in cell-to-cell communication and the orchestration of virulence in biomedically relevant pathogens. The alkylquinolone, 2-heptyl-4-quinolone (HHQ), was recently found to arrest cell growth without inducing cell mortality in selected phytoplankton species at nanomolar concentrations, suggesting QS molecules like HHQ can influence algal physiology, playing pivotal roles in structuring larger ecological frameworks. Results To understand how natural communities of phytoplankton and bacteria respond to HHQ, field-based incubation experiments with ecologically relevant concentrations of HHQ were conducted over the course of a stimulated phytoplankton bloom. Bulk flow cytometry measurements indicated that, in general, exposure to HHQ caused nanoplankton and prokaryotic cell abundances to decrease. Amplicon sequencing revealed HHQ exposure altered the composition of particle-associated and free-living microbiota, favoring the relative expansion of both gamma- and alpha-proteobacteria, and a concurrent decrease in Bacteroidetes. Specifically, Pseudoalteromonas spp., known to produce HHQ, increased in relative abundance following HHQ exposure. A search of representative bacterial genomes from genera that increased in relative abundance when exposed to HHQ revealed that they all have the genetic potential to bind HHQ. Conclusions This work demonstrates HHQ has the capacity to influence microbial community organization, suggesting alkylquinolones have functions beyond bacterial communication and are pivotal in driving microbial community structure and phytoplankton growth. Knowledge of how bacterial signals alter marine communities will serve to deepen our understanding of the impact these chemical interactions have on a global scale.
topic Quorum sensing
2-heptyl-4-quinolone
Microbiome
Phytoplankton
Pseudoalteromonas
url http://link.springer.com/article/10.1186/s40168-019-0711-9
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