A Widespread Bacterial Secretion System with Diverse Substrates

ABSTRACT In host-associated bacteria, surface and secreted proteins mediate acquisition of nutrients, interactions with host cells, and specificity of tissue localization. In Gram-negative bacteria, the mechanism by which many proteins cross and/or become tethered to the outer membrane remains uncle...

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Autores principales:	Alex S. Grossman, Terra J. Mauer, Katrina T. Forest, Heidi Goodrich-Blair
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	DUF560 HACEK HrpB NilB Slam Steinernema Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/361bdb1d08f840cf9fc9bf73e05bb91e
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spelling	oai:doaj.org-article:361bdb1d08f840cf9fc9bf73e05bb91e2021-11-10T18:37:52ZA Widespread Bacterial Secretion System with Diverse Substrates10.1128/mBio.01956-212150-7511https://doaj.org/article/361bdb1d08f840cf9fc9bf73e05bb91e2021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01956-21https://doaj.org/toc/2150-7511ABSTRACT In host-associated bacteria, surface and secreted proteins mediate acquisition of nutrients, interactions with host cells, and specificity of tissue localization. In Gram-negative bacteria, the mechanism by which many proteins cross and/or become tethered to the outer membrane remains unclear. The domain of unknown function 560 (DUF560) occurs in outer membrane proteins throughout Proteobacteria and has been implicated in host-bacterium interactions and lipoprotein surface exposure. We used sequence similarity networking to reveal three subfamilies of DUF560 homologs. One subfamily includes those DUF560 proteins experimentally characterized thus far: NilB, a host range determinant of the nematode-mutualist Xenorhabdus nematophila, and the surface lipoprotein assembly modulators Slam1 and Slam2, which facilitate lipoprotein surface exposure in Neisseria meningitidis (Y. Hooda, C. C. Lai, A. Judd, C. M. Buckwalter, et al., Nat Microbiol 1:16009, 2016, https://doi.org/10.1038/nmicrobiol.2016.9; Y. Hooda, C. C. L. Lai, T. F. Moraes, Front Cell Infect Microbiol 7:207, 2017, https://doi.org/10.3389/fcimb.2017.00207). We show that DUF560 proteins from a second subfamily facilitate secretion of soluble, nonlipidated proteins across the outer membrane. Using in silico analysis, we demonstrate that DUF560 gene complement correlates with bacterial environment at a macro level and host association at a species level. The DUF560 protein superfamily represents a newly characterized Gram-negative secretion system capable of lipoprotein surface exposure and soluble protein secretion with conserved roles in facilitating symbiosis. In light of these data, we propose that it be titled the type 11 secretion system (TXISS). IMPORTANCE The microbial constituency of a host-associated microbiome emerges from a complex physical and chemical interplay of microbial colonization factors, host surface conditions, and host immunological responses. To fill unique niches within a host, bacteria encode surface and secreted proteins that enable interactions with and responses to the host and co-occurring microbes. Bioinformatic predictions of putative bacterial colonization factor localization and function facilitate hypotheses about the potential of bacteria to engage in pathogenic, mutualistic, or commensal activities. This study uses publicly available genome sequence data alongside experimental results from Xenorhabdus nematophila to demonstrate a role for DUF560 family proteins in secretion of bacterial effectors of host interactions. Our research delineates a broadly distributed family of proteins and enables more accurate predictions of the localization of colonization factors throughout Proteobacteria.Alex S. GrossmanTerra J. MauerKatrina T. ForestHeidi Goodrich-BlairAmerican Society for MicrobiologyarticleDUF560HACEKHrpBNilBSlamSteinernemaMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	DUF560 HACEK HrpB NilB Slam Steinernema Microbiology QR1-502
spellingShingle	DUF560 HACEK HrpB NilB Slam Steinernema Microbiology QR1-502 Alex S. Grossman Terra J. Mauer Katrina T. Forest Heidi Goodrich-Blair A Widespread Bacterial Secretion System with Diverse Substrates
description	ABSTRACT In host-associated bacteria, surface and secreted proteins mediate acquisition of nutrients, interactions with host cells, and specificity of tissue localization. In Gram-negative bacteria, the mechanism by which many proteins cross and/or become tethered to the outer membrane remains unclear. The domain of unknown function 560 (DUF560) occurs in outer membrane proteins throughout Proteobacteria and has been implicated in host-bacterium interactions and lipoprotein surface exposure. We used sequence similarity networking to reveal three subfamilies of DUF560 homologs. One subfamily includes those DUF560 proteins experimentally characterized thus far: NilB, a host range determinant of the nematode-mutualist Xenorhabdus nematophila, and the surface lipoprotein assembly modulators Slam1 and Slam2, which facilitate lipoprotein surface exposure in Neisseria meningitidis (Y. Hooda, C. C. Lai, A. Judd, C. M. Buckwalter, et al., Nat Microbiol 1:16009, 2016, https://doi.org/10.1038/nmicrobiol.2016.9; Y. Hooda, C. C. L. Lai, T. F. Moraes, Front Cell Infect Microbiol 7:207, 2017, https://doi.org/10.3389/fcimb.2017.00207). We show that DUF560 proteins from a second subfamily facilitate secretion of soluble, nonlipidated proteins across the outer membrane. Using in silico analysis, we demonstrate that DUF560 gene complement correlates with bacterial environment at a macro level and host association at a species level. The DUF560 protein superfamily represents a newly characterized Gram-negative secretion system capable of lipoprotein surface exposure and soluble protein secretion with conserved roles in facilitating symbiosis. In light of these data, we propose that it be titled the type 11 secretion system (TXISS). IMPORTANCE The microbial constituency of a host-associated microbiome emerges from a complex physical and chemical interplay of microbial colonization factors, host surface conditions, and host immunological responses. To fill unique niches within a host, bacteria encode surface and secreted proteins that enable interactions with and responses to the host and co-occurring microbes. Bioinformatic predictions of putative bacterial colonization factor localization and function facilitate hypotheses about the potential of bacteria to engage in pathogenic, mutualistic, or commensal activities. This study uses publicly available genome sequence data alongside experimental results from Xenorhabdus nematophila to demonstrate a role for DUF560 family proteins in secretion of bacterial effectors of host interactions. Our research delineates a broadly distributed family of proteins and enables more accurate predictions of the localization of colonization factors throughout Proteobacteria.
format	article
author	Alex S. Grossman Terra J. Mauer Katrina T. Forest Heidi Goodrich-Blair
author_facet	Alex S. Grossman Terra J. Mauer Katrina T. Forest Heidi Goodrich-Blair
author_sort	Alex S. Grossman
title	A Widespread Bacterial Secretion System with Diverse Substrates
title_short	A Widespread Bacterial Secretion System with Diverse Substrates
title_full	A Widespread Bacterial Secretion System with Diverse Substrates
title_fullStr	A Widespread Bacterial Secretion System with Diverse Substrates
title_full_unstemmed	A Widespread Bacterial Secretion System with Diverse Substrates
title_sort	widespread bacterial secretion system with diverse substrates
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/361bdb1d08f840cf9fc9bf73e05bb91e
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A Widespread Bacterial Secretion System with Diverse Substrates

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