Investigation of the Genetics and Biochemistry of Roseobacticide Production in the <italic toggle="yes">Roseobacter</italic> Clade Bacterium <named-content content-type="genus-species">Phaeobacter inhibens</named-content>

ABSTRACT Roseobacter clade bacteria are abundant in surface waters and are among the most metabolically diverse and ecologically significant species. This group includes opportunistic symbionts that associate with micro- and macroalgae. We have proposed that one representative member, Phaeobacter in...

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Autores principales:	Rurun Wang, Étienne Gallant, Mohammad R. Seyedsayamdost
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d688cb7cebfe43bba1f672ea6b01e6da
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spelling	oai:doaj.org-article:d688cb7cebfe43bba1f672ea6b01e6da2021-11-15T15:41:41ZInvestigation of the Genetics and Biochemistry of Roseobacticide Production in the <italic toggle="yes">Roseobacter</italic> Clade Bacterium <named-content content-type="genus-species">Phaeobacter inhibens</named-content>10.1128/mBio.02118-152150-7511https://doaj.org/article/d688cb7cebfe43bba1f672ea6b01e6da2016-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02118-15https://doaj.org/toc/2150-7511ABSTRACT Roseobacter clade bacteria are abundant in surface waters and are among the most metabolically diverse and ecologically significant species. This group includes opportunistic symbionts that associate with micro- and macroalgae. We have proposed that one representative member, Phaeobacter inhibens, engages in a dynamic symbiosis with the microalga Emiliania huxleyi. In one phase, mutualistically beneficial molecules are exchanged, including the Roseobacter-produced antibiotic tropodithietic acid (TDA), which is thought to protect the symbiotic interaction. In an alternative parasitic phase, triggered by algal senescence, the bacteria produce potent algaecides, the roseobacticides, which kill the algal host. Here, we employed genetic and biochemical screens to identify the roseobacticide biosynthetic gene cluster. By using a transposon mutagenesis approach, we found that genes required for TDA synthesis—the tda operon and paa catabolon—are also necessary for roseobacticide production. Thus, in contrast to the one-cluster–one-compound paradigm, the tda gene cluster can generate two sets of molecules with distinct structures and bioactivities. We further show that roseobacticide production is quorum sensing regulated via an N-acyl homoserine lactone signal (3-OH–C10-HSL). To ensure tight regulation of algaecide production, and thus of a lifestyle switch from mutualism to parasitism, roseobacticide biosynthesis necessitates the presence of both an algal senescence molecule and a quorum sensing signal. IMPORTANCE Marine Roseobacter species are abundant in the oceans and engage in symbiotic interactions with microscopic algae. One member, P. inhibens, produces the antibiotic TDA and a growth hormone thought to protect and promote algal growth. However, in the presence of molecules released by senescing algae, the bacteria produce potent algaecides, the roseobacticides, which kill the host. We examined the regulatory networks and biosynthetic genes required for roseobacticide production. We found that P. inhibens uses largely the same set of genes for production of both TDA and roseobacticides, thus providing a rare case in which one gene cluster synthesizes two structurally and functionally distinct molecules. Moreover, we found roseobacticide production to be regulated by quorum sensing. Thus, two small molecules, the algal metabolite and the quorum-sensing signal, ensure tight control in the production of roseobacticides. These results highlight the role of small molecules in regulating microbial symbioses.Rurun WangÉtienne GallantMohammad R. SeyedsayamdostAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 2 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Rurun Wang Étienne Gallant Mohammad R. Seyedsayamdost Investigation of the Genetics and Biochemistry of Roseobacticide Production in the <italic toggle="yes">Roseobacter</italic> Clade Bacterium <named-content content-type="genus-species">Phaeobacter inhibens</named-content>
description	ABSTRACT Roseobacter clade bacteria are abundant in surface waters and are among the most metabolically diverse and ecologically significant species. This group includes opportunistic symbionts that associate with micro- and macroalgae. We have proposed that one representative member, Phaeobacter inhibens, engages in a dynamic symbiosis with the microalga Emiliania huxleyi. In one phase, mutualistically beneficial molecules are exchanged, including the Roseobacter-produced antibiotic tropodithietic acid (TDA), which is thought to protect the symbiotic interaction. In an alternative parasitic phase, triggered by algal senescence, the bacteria produce potent algaecides, the roseobacticides, which kill the algal host. Here, we employed genetic and biochemical screens to identify the roseobacticide biosynthetic gene cluster. By using a transposon mutagenesis approach, we found that genes required for TDA synthesis—the tda operon and paa catabolon—are also necessary for roseobacticide production. Thus, in contrast to the one-cluster–one-compound paradigm, the tda gene cluster can generate two sets of molecules with distinct structures and bioactivities. We further show that roseobacticide production is quorum sensing regulated via an N-acyl homoserine lactone signal (3-OH–C10-HSL). To ensure tight regulation of algaecide production, and thus of a lifestyle switch from mutualism to parasitism, roseobacticide biosynthesis necessitates the presence of both an algal senescence molecule and a quorum sensing signal. IMPORTANCE Marine Roseobacter species are abundant in the oceans and engage in symbiotic interactions with microscopic algae. One member, P. inhibens, produces the antibiotic TDA and a growth hormone thought to protect and promote algal growth. However, in the presence of molecules released by senescing algae, the bacteria produce potent algaecides, the roseobacticides, which kill the host. We examined the regulatory networks and biosynthetic genes required for roseobacticide production. We found that P. inhibens uses largely the same set of genes for production of both TDA and roseobacticides, thus providing a rare case in which one gene cluster synthesizes two structurally and functionally distinct molecules. Moreover, we found roseobacticide production to be regulated by quorum sensing. Thus, two small molecules, the algal metabolite and the quorum-sensing signal, ensure tight control in the production of roseobacticides. These results highlight the role of small molecules in regulating microbial symbioses.
format	article
author	Rurun Wang Étienne Gallant Mohammad R. Seyedsayamdost
author_facet	Rurun Wang Étienne Gallant Mohammad R. Seyedsayamdost
author_sort	Rurun Wang
title	Investigation of the Genetics and Biochemistry of Roseobacticide Production in the <italic toggle="yes">Roseobacter</italic> Clade Bacterium <named-content content-type="genus-species">Phaeobacter inhibens</named-content>
title_short	Investigation of the Genetics and Biochemistry of Roseobacticide Production in the <italic toggle="yes">Roseobacter</italic> Clade Bacterium <named-content content-type="genus-species">Phaeobacter inhibens</named-content>
title_full	Investigation of the Genetics and Biochemistry of Roseobacticide Production in the <italic toggle="yes">Roseobacter</italic> Clade Bacterium <named-content content-type="genus-species">Phaeobacter inhibens</named-content>
title_fullStr	Investigation of the Genetics and Biochemistry of Roseobacticide Production in the <italic toggle="yes">Roseobacter</italic> Clade Bacterium <named-content content-type="genus-species">Phaeobacter inhibens</named-content>
title_full_unstemmed	Investigation of the Genetics and Biochemistry of Roseobacticide Production in the <italic toggle="yes">Roseobacter</italic> Clade Bacterium <named-content content-type="genus-species">Phaeobacter inhibens</named-content>
title_sort	investigation of the genetics and biochemistry of roseobacticide production in the <italic toggle="yes">roseobacter</italic> clade bacterium <named-content content-type="genus-species">phaeobacter inhibens</named-content>
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/d688cb7cebfe43bba1f672ea6b01e6da
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Investigation of the Genetics and Biochemistry of Roseobacticide Production in the <italic toggle="yes">Roseobacter</italic> Clade Bacterium <named-content content-type="genus-species">Phaeobacter inhibens</named-content>

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