VxrB Influences Antagonism within Biofilms by Controlling Competition through Extracellular Matrix Production and Type 6 Secretion

ABSTRACT The human pathogen Vibrio cholerae grows as biofilms, communities of cells encased in an extracellular matrix. When growing in biofilms, cells compete for resources and space. One common competitive mechanism among Gram-negative bacteria is the type six secretion system (T6SS), which can deliver toxic effector proteins into a diverse group of target cells, including other bacteria, phagocytic amoebas, and human macrophages. The response regulator VxrB positively regulates both biofilm matrix and T6SS gene expression. Here, we directly observe T6SS activity within biofilms, which results in improved competition with strains lacking the T6SS. VxrB significantly contributes to both attack and defense via T6SS, while also influencing competition via regulation of biofilm matrix production. We further determined that both Vibrio polysaccharide (VPS) and the biofilm matrix protein RbmA can protect cells from T6SS attack within mature biofilms. By varying the spatial mixing of predator and prey cells in biofilms, we show that a high degree of mixing favors T6SS predator strains and that the presence of extracellular DNA in V. cholerae biofilms is a signature of T6SS killing. VxrB therefore regulates both T6SS attack and matrix-based T6SS defense, to control antagonistic interactions and competition outcomes during mixed-strain biofilm formation. IMPORTANCE This work demonstrates that the Vibrio cholerae type six secretion system (T6SS) can actively kill prey strains within the interior of biofilm populations with substantial impact on population dynamics. We additionally show that the response regulator VxrB contributes to both T6SS killing and protection from T6SS killing within biofilms. Components of the biofilm matrix and the degree of spatial mixing among strains also strongly influence T6SS competition dynamics. T6SS killing within biofilms results in increased localized release of extracellular DNA, which serves as an additional matrix component. These findings collectively demonstrate that T6SS killing can contribute to competition within biofilms and that this competition depends on key regulators, matrix components, and the extent of spatial population mixture during biofilm growth. Ausführliche Beschreibung

Gespeichert in:

Autor*in:	Jennifer K. Teschler [verfasserIn] Eva Jiménez-Siebert [verfasserIn] Hannah Jeckel [verfasserIn] Praveen K. Singh [verfasserIn] Jin Hwan Park [verfasserIn] Stefan Pukatzki [verfasserIn] Carey D. Nadell [verfasserIn] Knut Drescher [verfasserIn] Fitnat H. Yildiz [verfasserIn]

Format:	E-Artikel
Sprache:	Englisch

Erschienen:	2022

Schlagwörter:	Vibrio cholerae biofilm type six secretion system

Übergeordnetes Werk:	In: mBio - American Society for Microbiology, 2010, 13(2022), 4
Übergeordnetes Werk:	volume:13 ; year:2022 ; number:4

Links:	Link aufrufen Link aufrufen Link aufrufen Journal toc

DOI / URN:	10.1128/mbio.01885-22

Katalog-ID:	DOAJ084671424

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allfields	10.1128/mbio.01885-22 doi (DE-627)DOAJ084671424 (DE-599)DOAJ964f624d3b414a30862f81f9ffbffbd6 DE-627 ger DE-627 rakwb eng QR1-502 Jennifer K. Teschler verfasserin aut VxrB Influences Antagonism within Biofilms by Controlling Competition through Extracellular Matrix Production and Type 6 Secretion 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT The human pathogen Vibrio cholerae grows as biofilms, communities of cells encased in an extracellular matrix. When growing in biofilms, cells compete for resources and space. One common competitive mechanism among Gram-negative bacteria is the type six secretion system (T6SS), which can deliver toxic effector proteins into a diverse group of target cells, including other bacteria, phagocytic amoebas, and human macrophages. The response regulator VxrB positively regulates both biofilm matrix and T6SS gene expression. Here, we directly observe T6SS activity within biofilms, which results in improved competition with strains lacking the T6SS. VxrB significantly contributes to both attack and defense via T6SS, while also influencing competition via regulation of biofilm matrix production. We further determined that both Vibrio polysaccharide (VPS) and the biofilm matrix protein RbmA can protect cells from T6SS attack within mature biofilms. By varying the spatial mixing of predator and prey cells in biofilms, we show that a high degree of mixing favors T6SS predator strains and that the presence of extracellular DNA in V. cholerae biofilms is a signature of T6SS killing. VxrB therefore regulates both T6SS attack and matrix-based T6SS defense, to control antagonistic interactions and competition outcomes during mixed-strain biofilm formation. IMPORTANCE This work demonstrates that the Vibrio cholerae type six secretion system (T6SS) can actively kill prey strains within the interior of biofilm populations with substantial impact on population dynamics. We additionally show that the response regulator VxrB contributes to both T6SS killing and protection from T6SS killing within biofilms. Components of the biofilm matrix and the degree of spatial mixing among strains also strongly influence T6SS competition dynamics. T6SS killing within biofilms results in increased localized release of extracellular DNA, which serves as an additional matrix component. These findings collectively demonstrate that T6SS killing can contribute to competition within biofilms and that this competition depends on key regulators, matrix components, and the extent of spatial population mixture during biofilm growth. Vibrio cholerae biofilm type six secretion system Microbiology Eva Jiménez-Siebert verfasserin aut Hannah Jeckel verfasserin aut Praveen K. Singh verfasserin aut Jin Hwan Park verfasserin aut Stefan Pukatzki verfasserin aut Carey D. Nadell verfasserin aut Knut Drescher verfasserin aut Fitnat H. Yildiz verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 4 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:4 https://doi.org/10.1128/mbio.01885-22 kostenfrei https://doaj.org/article/964f624d3b414a30862f81f9ffbffbd6 kostenfrei https://journals.asm.org/doi/10.1128/mbio.01885-22 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 4
spelling	10.1128/mbio.01885-22 doi (DE-627)DOAJ084671424 (DE-599)DOAJ964f624d3b414a30862f81f9ffbffbd6 DE-627 ger DE-627 rakwb eng QR1-502 Jennifer K. Teschler verfasserin aut VxrB Influences Antagonism within Biofilms by Controlling Competition through Extracellular Matrix Production and Type 6 Secretion 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT The human pathogen Vibrio cholerae grows as biofilms, communities of cells encased in an extracellular matrix. When growing in biofilms, cells compete for resources and space. One common competitive mechanism among Gram-negative bacteria is the type six secretion system (T6SS), which can deliver toxic effector proteins into a diverse group of target cells, including other bacteria, phagocytic amoebas, and human macrophages. The response regulator VxrB positively regulates both biofilm matrix and T6SS gene expression. Here, we directly observe T6SS activity within biofilms, which results in improved competition with strains lacking the T6SS. VxrB significantly contributes to both attack and defense via T6SS, while also influencing competition via regulation of biofilm matrix production. We further determined that both Vibrio polysaccharide (VPS) and the biofilm matrix protein RbmA can protect cells from T6SS attack within mature biofilms. By varying the spatial mixing of predator and prey cells in biofilms, we show that a high degree of mixing favors T6SS predator strains and that the presence of extracellular DNA in V. cholerae biofilms is a signature of T6SS killing. VxrB therefore regulates both T6SS attack and matrix-based T6SS defense, to control antagonistic interactions and competition outcomes during mixed-strain biofilm formation. IMPORTANCE This work demonstrates that the Vibrio cholerae type six secretion system (T6SS) can actively kill prey strains within the interior of biofilm populations with substantial impact on population dynamics. We additionally show that the response regulator VxrB contributes to both T6SS killing and protection from T6SS killing within biofilms. Components of the biofilm matrix and the degree of spatial mixing among strains also strongly influence T6SS competition dynamics. T6SS killing within biofilms results in increased localized release of extracellular DNA, which serves as an additional matrix component. These findings collectively demonstrate that T6SS killing can contribute to competition within biofilms and that this competition depends on key regulators, matrix components, and the extent of spatial population mixture during biofilm growth. Vibrio cholerae biofilm type six secretion system Microbiology Eva Jiménez-Siebert verfasserin aut Hannah Jeckel verfasserin aut Praveen K. Singh verfasserin aut Jin Hwan Park verfasserin aut Stefan Pukatzki verfasserin aut Carey D. Nadell verfasserin aut Knut Drescher verfasserin aut Fitnat H. Yildiz verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 4 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:4 https://doi.org/10.1128/mbio.01885-22 kostenfrei https://doaj.org/article/964f624d3b414a30862f81f9ffbffbd6 kostenfrei https://journals.asm.org/doi/10.1128/mbio.01885-22 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 4
allfields_unstemmed	10.1128/mbio.01885-22 doi (DE-627)DOAJ084671424 (DE-599)DOAJ964f624d3b414a30862f81f9ffbffbd6 DE-627 ger DE-627 rakwb eng QR1-502 Jennifer K. Teschler verfasserin aut VxrB Influences Antagonism within Biofilms by Controlling Competition through Extracellular Matrix Production and Type 6 Secretion 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT The human pathogen Vibrio cholerae grows as biofilms, communities of cells encased in an extracellular matrix. When growing in biofilms, cells compete for resources and space. One common competitive mechanism among Gram-negative bacteria is the type six secretion system (T6SS), which can deliver toxic effector proteins into a diverse group of target cells, including other bacteria, phagocytic amoebas, and human macrophages. The response regulator VxrB positively regulates both biofilm matrix and T6SS gene expression. Here, we directly observe T6SS activity within biofilms, which results in improved competition with strains lacking the T6SS. VxrB significantly contributes to both attack and defense via T6SS, while also influencing competition via regulation of biofilm matrix production. We further determined that both Vibrio polysaccharide (VPS) and the biofilm matrix protein RbmA can protect cells from T6SS attack within mature biofilms. By varying the spatial mixing of predator and prey cells in biofilms, we show that a high degree of mixing favors T6SS predator strains and that the presence of extracellular DNA in V. cholerae biofilms is a signature of T6SS killing. VxrB therefore regulates both T6SS attack and matrix-based T6SS defense, to control antagonistic interactions and competition outcomes during mixed-strain biofilm formation. IMPORTANCE This work demonstrates that the Vibrio cholerae type six secretion system (T6SS) can actively kill prey strains within the interior of biofilm populations with substantial impact on population dynamics. We additionally show that the response regulator VxrB contributes to both T6SS killing and protection from T6SS killing within biofilms. Components of the biofilm matrix and the degree of spatial mixing among strains also strongly influence T6SS competition dynamics. T6SS killing within biofilms results in increased localized release of extracellular DNA, which serves as an additional matrix component. These findings collectively demonstrate that T6SS killing can contribute to competition within biofilms and that this competition depends on key regulators, matrix components, and the extent of spatial population mixture during biofilm growth. Vibrio cholerae biofilm type six secretion system Microbiology Eva Jiménez-Siebert verfasserin aut Hannah Jeckel verfasserin aut Praveen K. Singh verfasserin aut Jin Hwan Park verfasserin aut Stefan Pukatzki verfasserin aut Carey D. Nadell verfasserin aut Knut Drescher verfasserin aut Fitnat H. Yildiz verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 4 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:4 https://doi.org/10.1128/mbio.01885-22 kostenfrei https://doaj.org/article/964f624d3b414a30862f81f9ffbffbd6 kostenfrei https://journals.asm.org/doi/10.1128/mbio.01885-22 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 4
allfieldsGer	10.1128/mbio.01885-22 doi (DE-627)DOAJ084671424 (DE-599)DOAJ964f624d3b414a30862f81f9ffbffbd6 DE-627 ger DE-627 rakwb eng QR1-502 Jennifer K. Teschler verfasserin aut VxrB Influences Antagonism within Biofilms by Controlling Competition through Extracellular Matrix Production and Type 6 Secretion 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT The human pathogen Vibrio cholerae grows as biofilms, communities of cells encased in an extracellular matrix. When growing in biofilms, cells compete for resources and space. One common competitive mechanism among Gram-negative bacteria is the type six secretion system (T6SS), which can deliver toxic effector proteins into a diverse group of target cells, including other bacteria, phagocytic amoebas, and human macrophages. The response regulator VxrB positively regulates both biofilm matrix and T6SS gene expression. Here, we directly observe T6SS activity within biofilms, which results in improved competition with strains lacking the T6SS. VxrB significantly contributes to both attack and defense via T6SS, while also influencing competition via regulation of biofilm matrix production. We further determined that both Vibrio polysaccharide (VPS) and the biofilm matrix protein RbmA can protect cells from T6SS attack within mature biofilms. By varying the spatial mixing of predator and prey cells in biofilms, we show that a high degree of mixing favors T6SS predator strains and that the presence of extracellular DNA in V. cholerae biofilms is a signature of T6SS killing. VxrB therefore regulates both T6SS attack and matrix-based T6SS defense, to control antagonistic interactions and competition outcomes during mixed-strain biofilm formation. IMPORTANCE This work demonstrates that the Vibrio cholerae type six secretion system (T6SS) can actively kill prey strains within the interior of biofilm populations with substantial impact on population dynamics. We additionally show that the response regulator VxrB contributes to both T6SS killing and protection from T6SS killing within biofilms. Components of the biofilm matrix and the degree of spatial mixing among strains also strongly influence T6SS competition dynamics. T6SS killing within biofilms results in increased localized release of extracellular DNA, which serves as an additional matrix component. These findings collectively demonstrate that T6SS killing can contribute to competition within biofilms and that this competition depends on key regulators, matrix components, and the extent of spatial population mixture during biofilm growth. Vibrio cholerae biofilm type six secretion system Microbiology Eva Jiménez-Siebert verfasserin aut Hannah Jeckel verfasserin aut Praveen K. Singh verfasserin aut Jin Hwan Park verfasserin aut Stefan Pukatzki verfasserin aut Carey D. Nadell verfasserin aut Knut Drescher verfasserin aut Fitnat H. Yildiz verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 4 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:4 https://doi.org/10.1128/mbio.01885-22 kostenfrei https://doaj.org/article/964f624d3b414a30862f81f9ffbffbd6 kostenfrei https://journals.asm.org/doi/10.1128/mbio.01885-22 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 4
allfieldsSound	10.1128/mbio.01885-22 doi (DE-627)DOAJ084671424 (DE-599)DOAJ964f624d3b414a30862f81f9ffbffbd6 DE-627 ger DE-627 rakwb eng QR1-502 Jennifer K. Teschler verfasserin aut VxrB Influences Antagonism within Biofilms by Controlling Competition through Extracellular Matrix Production and Type 6 Secretion 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT The human pathogen Vibrio cholerae grows as biofilms, communities of cells encased in an extracellular matrix. When growing in biofilms, cells compete for resources and space. One common competitive mechanism among Gram-negative bacteria is the type six secretion system (T6SS), which can deliver toxic effector proteins into a diverse group of target cells, including other bacteria, phagocytic amoebas, and human macrophages. The response regulator VxrB positively regulates both biofilm matrix and T6SS gene expression. Here, we directly observe T6SS activity within biofilms, which results in improved competition with strains lacking the T6SS. VxrB significantly contributes to both attack and defense via T6SS, while also influencing competition via regulation of biofilm matrix production. We further determined that both Vibrio polysaccharide (VPS) and the biofilm matrix protein RbmA can protect cells from T6SS attack within mature biofilms. By varying the spatial mixing of predator and prey cells in biofilms, we show that a high degree of mixing favors T6SS predator strains and that the presence of extracellular DNA in V. cholerae biofilms is a signature of T6SS killing. VxrB therefore regulates both T6SS attack and matrix-based T6SS defense, to control antagonistic interactions and competition outcomes during mixed-strain biofilm formation. IMPORTANCE This work demonstrates that the Vibrio cholerae type six secretion system (T6SS) can actively kill prey strains within the interior of biofilm populations with substantial impact on population dynamics. We additionally show that the response regulator VxrB contributes to both T6SS killing and protection from T6SS killing within biofilms. Components of the biofilm matrix and the degree of spatial mixing among strains also strongly influence T6SS competition dynamics. T6SS killing within biofilms results in increased localized release of extracellular DNA, which serves as an additional matrix component. These findings collectively demonstrate that T6SS killing can contribute to competition within biofilms and that this competition depends on key regulators, matrix components, and the extent of spatial population mixture during biofilm growth. Vibrio cholerae biofilm type six secretion system Microbiology Eva Jiménez-Siebert verfasserin aut Hannah Jeckel verfasserin aut Praveen K. Singh verfasserin aut Jin Hwan Park verfasserin aut Stefan Pukatzki verfasserin aut Carey D. Nadell verfasserin aut Knut Drescher verfasserin aut Fitnat H. Yildiz verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 4 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:4 https://doi.org/10.1128/mbio.01885-22 kostenfrei https://doaj.org/article/964f624d3b414a30862f81f9ffbffbd6 kostenfrei https://journals.asm.org/doi/10.1128/mbio.01885-22 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 4
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authorswithroles_txt_mv	Jennifer K. Teschler @@aut@@ Eva Jiménez-Siebert @@aut@@ Hannah Jeckel @@aut@@ Praveen K. Singh @@aut@@ Jin Hwan Park @@aut@@ Stefan Pukatzki @@aut@@ Carey D. Nadell @@aut@@ Knut Drescher @@aut@@ Fitnat H. Yildiz @@aut@@
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author	Jennifer K. Teschler
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title	VxrB Influences Antagonism within Biofilms by Controlling Competition through Extracellular Matrix Production and Type 6 Secretion
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title_full	VxrB Influences Antagonism within Biofilms by Controlling Competition through Extracellular Matrix Production and Type 6 Secretion
author_sort	Jennifer K. Teschler
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author_browse	Jennifer K. Teschler Eva Jiménez-Siebert Hannah Jeckel Praveen K. Singh Jin Hwan Park Stefan Pukatzki Carey D. Nadell Knut Drescher Fitnat H. Yildiz
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author-letter	Jennifer K. Teschler
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title_sort	vxrb influences antagonism within biofilms by controlling competition through extracellular matrix production and type 6 secretion
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title_auth	VxrB Influences Antagonism within Biofilms by Controlling Competition through Extracellular Matrix Production and Type 6 Secretion
abstract	ABSTRACT The human pathogen Vibrio cholerae grows as biofilms, communities of cells encased in an extracellular matrix. When growing in biofilms, cells compete for resources and space. One common competitive mechanism among Gram-negative bacteria is the type six secretion system (T6SS), which can deliver toxic effector proteins into a diverse group of target cells, including other bacteria, phagocytic amoebas, and human macrophages. The response regulator VxrB positively regulates both biofilm matrix and T6SS gene expression. Here, we directly observe T6SS activity within biofilms, which results in improved competition with strains lacking the T6SS. VxrB significantly contributes to both attack and defense via T6SS, while also influencing competition via regulation of biofilm matrix production. We further determined that both Vibrio polysaccharide (VPS) and the biofilm matrix protein RbmA can protect cells from T6SS attack within mature biofilms. By varying the spatial mixing of predator and prey cells in biofilms, we show that a high degree of mixing favors T6SS predator strains and that the presence of extracellular DNA in V. cholerae biofilms is a signature of T6SS killing. VxrB therefore regulates both T6SS attack and matrix-based T6SS defense, to control antagonistic interactions and competition outcomes during mixed-strain biofilm formation. IMPORTANCE This work demonstrates that the Vibrio cholerae type six secretion system (T6SS) can actively kill prey strains within the interior of biofilm populations with substantial impact on population dynamics. We additionally show that the response regulator VxrB contributes to both T6SS killing and protection from T6SS killing within biofilms. Components of the biofilm matrix and the degree of spatial mixing among strains also strongly influence T6SS competition dynamics. T6SS killing within biofilms results in increased localized release of extracellular DNA, which serves as an additional matrix component. These findings collectively demonstrate that T6SS killing can contribute to competition within biofilms and that this competition depends on key regulators, matrix components, and the extent of spatial population mixture during biofilm growth.
abstractGer	ABSTRACT The human pathogen Vibrio cholerae grows as biofilms, communities of cells encased in an extracellular matrix. When growing in biofilms, cells compete for resources and space. One common competitive mechanism among Gram-negative bacteria is the type six secretion system (T6SS), which can deliver toxic effector proteins into a diverse group of target cells, including other bacteria, phagocytic amoebas, and human macrophages. The response regulator VxrB positively regulates both biofilm matrix and T6SS gene expression. Here, we directly observe T6SS activity within biofilms, which results in improved competition with strains lacking the T6SS. VxrB significantly contributes to both attack and defense via T6SS, while also influencing competition via regulation of biofilm matrix production. We further determined that both Vibrio polysaccharide (VPS) and the biofilm matrix protein RbmA can protect cells from T6SS attack within mature biofilms. By varying the spatial mixing of predator and prey cells in biofilms, we show that a high degree of mixing favors T6SS predator strains and that the presence of extracellular DNA in V. cholerae biofilms is a signature of T6SS killing. VxrB therefore regulates both T6SS attack and matrix-based T6SS defense, to control antagonistic interactions and competition outcomes during mixed-strain biofilm formation. IMPORTANCE This work demonstrates that the Vibrio cholerae type six secretion system (T6SS) can actively kill prey strains within the interior of biofilm populations with substantial impact on population dynamics. We additionally show that the response regulator VxrB contributes to both T6SS killing and protection from T6SS killing within biofilms. Components of the biofilm matrix and the degree of spatial mixing among strains also strongly influence T6SS competition dynamics. T6SS killing within biofilms results in increased localized release of extracellular DNA, which serves as an additional matrix component. These findings collectively demonstrate that T6SS killing can contribute to competition within biofilms and that this competition depends on key regulators, matrix components, and the extent of spatial population mixture during biofilm growth.
abstract_unstemmed	ABSTRACT The human pathogen Vibrio cholerae grows as biofilms, communities of cells encased in an extracellular matrix. When growing in biofilms, cells compete for resources and space. One common competitive mechanism among Gram-negative bacteria is the type six secretion system (T6SS), which can deliver toxic effector proteins into a diverse group of target cells, including other bacteria, phagocytic amoebas, and human macrophages. The response regulator VxrB positively regulates both biofilm matrix and T6SS gene expression. Here, we directly observe T6SS activity within biofilms, which results in improved competition with strains lacking the T6SS. VxrB significantly contributes to both attack and defense via T6SS, while also influencing competition via regulation of biofilm matrix production. We further determined that both Vibrio polysaccharide (VPS) and the biofilm matrix protein RbmA can protect cells from T6SS attack within mature biofilms. By varying the spatial mixing of predator and prey cells in biofilms, we show that a high degree of mixing favors T6SS predator strains and that the presence of extracellular DNA in V. cholerae biofilms is a signature of T6SS killing. VxrB therefore regulates both T6SS attack and matrix-based T6SS defense, to control antagonistic interactions and competition outcomes during mixed-strain biofilm formation. IMPORTANCE This work demonstrates that the Vibrio cholerae type six secretion system (T6SS) can actively kill prey strains within the interior of biofilm populations with substantial impact on population dynamics. We additionally show that the response regulator VxrB contributes to both T6SS killing and protection from T6SS killing within biofilms. Components of the biofilm matrix and the degree of spatial mixing among strains also strongly influence T6SS competition dynamics. T6SS killing within biofilms results in increased localized release of extracellular DNA, which serves as an additional matrix component. These findings collectively demonstrate that T6SS killing can contribute to competition within biofilms and that this competition depends on key regulators, matrix components, and the extent of spatial population mixture during biofilm growth.
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title_short	VxrB Influences Antagonism within Biofilms by Controlling Competition through Extracellular Matrix Production and Type 6 Secretion
url	https://doi.org/10.1128/mbio.01885-22 https://doaj.org/article/964f624d3b414a30862f81f9ffbffbd6 https://journals.asm.org/doi/10.1128/mbio.01885-22 https://doaj.org/toc/2150-7511
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author2	Eva Jiménez-Siebert Hannah Jeckel Praveen K. Singh Jin Hwan Park Stefan Pukatzki Carey D. Nadell Knut Drescher Fitnat H. Yildiz
author2Str	Eva Jiménez-Siebert Hannah Jeckel Praveen K. Singh Jin Hwan Park Stefan Pukatzki Carey D. Nadell Knut Drescher Fitnat H. Yildiz
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doi_str	10.1128/mbio.01885-22
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up_date	2024-07-04T00:04:27.830Z
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