publication . Article . 2017

Diversification of Type VI Secretion System Toxins Reveals Ancient Antagonism among Bee Gut Microbes

Steele, Margaret I.; Kwong, Waldan K.; Whiteley, Marvin; Moran, Nancy A.;
Open Access English
  • Published: 01 Dec 2017 Journal: mBio, volume 8, issue 6 (eissn: 2150-7511, Copyright policy)
  • Publisher: American Society for Microbiology
Abstract
ABSTRACT Microbial communities are shaped by interactions among their constituent members. Some Gram-negative bacteria employ type VI secretion systems (T6SSs) to inject protein toxins into neighboring cells. These interactions have been theorized to affect the composition of host-associated microbiomes, but the role of T6SSs in the evolution of gut communities is not well understood. We report the discovery of two T6SSs and numerous T6SS-associated Rhs toxins within the gut bacteria of honey bees and bumble bees. We sequenced the genomes of 28 strains of Snodgrassella alvi, a characteristic bee gut microbe, and found tremendous variability in their Rhs toxin co...
Subjects
free text keywords: Research Article, Snodgrassella alvi, coevolution, Apis mellifera, Bombus, Rhs toxin
Funded by
NSF| Dimensions: Genomics, functional roles, and diversity of the symbiotic gut microbiotae of honey bees and bumble bees
Project
  • Funder: National Science Foundation (NSF)
  • Project Code: 1415604
  • Funding stream: Directorate for Biological Sciences | Division of Environmental Biology
,
NSF| DISSERTATION RESEARCH: Competition and cooperation in the honey bee gut microbiota
Project
  • Funder: National Science Foundation (NSF)
  • Project Code: 1701430
  • Funding stream: Directorate for Biological Sciences | Division of Environmental Biology
,
NIH| Host and symbiont determinants of colonization by a co-evolved gut community
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01GM108477-03
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
74 references, page 1 of 5

1.Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, Nelson WC, Heidelberg JF, Mekalanos JJ 2006 Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 103:1528–1533. doi:10.1073/pnas.0510322103.16432199 [OpenAIRE] [PubMed] [DOI]

2.Hood RD, Singh P, Hsu F, Güvener T, Carl MA, Trinidad RRS, Silverman JM, Ohlson BB, Hicks KG, Plemel RL, Li M, Schwarz S, Wang WY, Merz AJ, Goodlett DR, Mougous JD 2010 A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7:25–37. doi:10.1016/j.chom.2009.12.007.20114026 [OpenAIRE] [PubMed] [DOI]

3.Cascales E, Cambillau C 2012 Structural biology of type VI secretion systems. Philos Trans R Soc Lond B Biol Sci 367:1102–1111. doi:10.1098/rstb.2011.0209.22411981 [OpenAIRE] [PubMed] [DOI]

4.Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ 2012 Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483:182–186. doi:10.1038/nature10846.22367545 [OpenAIRE] [PubMed] [DOI]

5.McNally L, Bernardy E, Thomas J, Kalziqi A, Pentz J, Brown SP, Hammer BK, Yunker PJ, Ratcliff WC 2017 Killing by type VI secretion drives genetic phase separation and correlates with increased cooperation. Nat Commun 8:14371. doi:10.1038/ncomms14371.28165005 [OpenAIRE] [PubMed] [DOI]

6.Wong M, Liang X, Smart M, Tang L, Moore R, Ingalls B, Dong TG 2016 Microbial herd protection mediated by antagonistic interaction in polymicrobial communities. Appl Environ Microbiol 82:6881–6888. doi:10.1128/AEM.02210-16. [OpenAIRE] [DOI]

7.Russell AB, Wexler AG, Harding BN, Whitney JC, Bohn AJ, Goo YA, Tran BQ, Barry NA, Zheng H, Peterson SB, Chou S, Gonen T, Goodlett DR, Goodman AL, Mougous JD 2014 A type VI secretion-related pathway in Bacteroidetes mediates interbacterial antagonism. Cell Host Microbe 16:227–236. doi:10.1016/j.chom.2014.07.007.25070807 [OpenAIRE] [PubMed] [DOI]

8.Wexler AG, Bao Y, Whitney JC, Bobay LM, Xavier JB, Schofield WB, Barry NA, Russell AB, Tran BQ, Goo YA, Goodlett DR, Ochman H, Mougous JD, Goodman AL 2016 Human symbionts inject and neutralize antibacterial toxins to persist in the gut. Proc Natl Acad Sci U S A 113:3639–3644. doi:10.1073/pnas.1525637113.26957597 [OpenAIRE] [PubMed] [DOI]

9.Chatzidaki-Livanis M, Geva-Zatorsky N, Comstock LE 2016 Bacteroides fragilis type VI secretion systems use novel effector and immunity proteins to antagonize human gut Bacteroidales species. Proc Natl Acad Sci U S A 113:3627–3632. doi:10.1073/pnas.1522510113.26951680 [OpenAIRE] [PubMed] [DOI]

10.Verster AJ, Ross BD, Radey MC, Bao Y, Goodman AL, Mougous JD, Borenstein E 2017 The landscape of type VI secretion across human gut microbiomes reveals its role in community composition. Cell Host Microbe 22:411–419.e4. doi:10.1016/j.chom.2017.08.010.28910638 [OpenAIRE] [PubMed] [DOI]

11.Coyne MJ, Roelofs KG, Comstock LE 2016 Type VI secretion systems of human gut Bacteroidales segregate into three genetic architectures, two of which are contained on mobile genetic elements. BMC Genomics 17:58. doi:10.1186/s12864-016-2377-z.26768901 [OpenAIRE] [PubMed] [DOI]

12.Cariveau DP, Powell JE, Koch H, Winfree R, Moran NA 2014 Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). ISME J 8:2369–2379. doi:10.1038/ismej.2014.68.24763369 [OpenAIRE] [PubMed] [DOI]

13.Powell E, Ratnayeke N, Moran NA 2016 Strain diversity and host specificity in a specialized gut symbiont of honey bees and bumble bees. Mol Ecol 25:4461–4471. doi:10.1111/mec.13787.27482856 [OpenAIRE] [PubMed] [DOI]

14.Kwong WK, Moran NA 2016 Gut microbial communities of social bees. Nat Rev Microbiol 14:374–384. doi:10.1038/nrmicro.2016.43.27140688 [OpenAIRE] [PubMed] [DOI]

15.Zheng H, Powell JE, Steele MI, Dietrich C, Moran NA 2017 Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proc Natl Acad Sci U S A 114:4775–4780. doi:10.1073/pnas.1701819114.28420790 [OpenAIRE] [PubMed] [DOI]

74 references, page 1 of 5
Abstract
ABSTRACT Microbial communities are shaped by interactions among their constituent members. Some Gram-negative bacteria employ type VI secretion systems (T6SSs) to inject protein toxins into neighboring cells. These interactions have been theorized to affect the composition of host-associated microbiomes, but the role of T6SSs in the evolution of gut communities is not well understood. We report the discovery of two T6SSs and numerous T6SS-associated Rhs toxins within the gut bacteria of honey bees and bumble bees. We sequenced the genomes of 28 strains of Snodgrassella alvi, a characteristic bee gut microbe, and found tremendous variability in their Rhs toxin co...
Subjects
free text keywords: Research Article, Snodgrassella alvi, coevolution, Apis mellifera, Bombus, Rhs toxin
Funded by
NSF| Dimensions: Genomics, functional roles, and diversity of the symbiotic gut microbiotae of honey bees and bumble bees
Project
  • Funder: National Science Foundation (NSF)
  • Project Code: 1415604
  • Funding stream: Directorate for Biological Sciences | Division of Environmental Biology
,
NSF| DISSERTATION RESEARCH: Competition and cooperation in the honey bee gut microbiota
Project
  • Funder: National Science Foundation (NSF)
  • Project Code: 1701430
  • Funding stream: Directorate for Biological Sciences | Division of Environmental Biology
,
NIH| Host and symbiont determinants of colonization by a co-evolved gut community
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01GM108477-03
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
74 references, page 1 of 5

1.Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, Nelson WC, Heidelberg JF, Mekalanos JJ 2006 Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 103:1528–1533. doi:10.1073/pnas.0510322103.16432199 [OpenAIRE] [PubMed] [DOI]

2.Hood RD, Singh P, Hsu F, Güvener T, Carl MA, Trinidad RRS, Silverman JM, Ohlson BB, Hicks KG, Plemel RL, Li M, Schwarz S, Wang WY, Merz AJ, Goodlett DR, Mougous JD 2010 A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7:25–37. doi:10.1016/j.chom.2009.12.007.20114026 [OpenAIRE] [PubMed] [DOI]

3.Cascales E, Cambillau C 2012 Structural biology of type VI secretion systems. Philos Trans R Soc Lond B Biol Sci 367:1102–1111. doi:10.1098/rstb.2011.0209.22411981 [OpenAIRE] [PubMed] [DOI]

4.Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ 2012 Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483:182–186. doi:10.1038/nature10846.22367545 [OpenAIRE] [PubMed] [DOI]

5.McNally L, Bernardy E, Thomas J, Kalziqi A, Pentz J, Brown SP, Hammer BK, Yunker PJ, Ratcliff WC 2017 Killing by type VI secretion drives genetic phase separation and correlates with increased cooperation. Nat Commun 8:14371. doi:10.1038/ncomms14371.28165005 [OpenAIRE] [PubMed] [DOI]

6.Wong M, Liang X, Smart M, Tang L, Moore R, Ingalls B, Dong TG 2016 Microbial herd protection mediated by antagonistic interaction in polymicrobial communities. Appl Environ Microbiol 82:6881–6888. doi:10.1128/AEM.02210-16. [OpenAIRE] [DOI]

7.Russell AB, Wexler AG, Harding BN, Whitney JC, Bohn AJ, Goo YA, Tran BQ, Barry NA, Zheng H, Peterson SB, Chou S, Gonen T, Goodlett DR, Goodman AL, Mougous JD 2014 A type VI secretion-related pathway in Bacteroidetes mediates interbacterial antagonism. Cell Host Microbe 16:227–236. doi:10.1016/j.chom.2014.07.007.25070807 [OpenAIRE] [PubMed] [DOI]

8.Wexler AG, Bao Y, Whitney JC, Bobay LM, Xavier JB, Schofield WB, Barry NA, Russell AB, Tran BQ, Goo YA, Goodlett DR, Ochman H, Mougous JD, Goodman AL 2016 Human symbionts inject and neutralize antibacterial toxins to persist in the gut. Proc Natl Acad Sci U S A 113:3639–3644. doi:10.1073/pnas.1525637113.26957597 [OpenAIRE] [PubMed] [DOI]

9.Chatzidaki-Livanis M, Geva-Zatorsky N, Comstock LE 2016 Bacteroides fragilis type VI secretion systems use novel effector and immunity proteins to antagonize human gut Bacteroidales species. Proc Natl Acad Sci U S A 113:3627–3632. doi:10.1073/pnas.1522510113.26951680 [OpenAIRE] [PubMed] [DOI]

10.Verster AJ, Ross BD, Radey MC, Bao Y, Goodman AL, Mougous JD, Borenstein E 2017 The landscape of type VI secretion across human gut microbiomes reveals its role in community composition. Cell Host Microbe 22:411–419.e4. doi:10.1016/j.chom.2017.08.010.28910638 [OpenAIRE] [PubMed] [DOI]

11.Coyne MJ, Roelofs KG, Comstock LE 2016 Type VI secretion systems of human gut Bacteroidales segregate into three genetic architectures, two of which are contained on mobile genetic elements. BMC Genomics 17:58. doi:10.1186/s12864-016-2377-z.26768901 [OpenAIRE] [PubMed] [DOI]

12.Cariveau DP, Powell JE, Koch H, Winfree R, Moran NA 2014 Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). ISME J 8:2369–2379. doi:10.1038/ismej.2014.68.24763369 [OpenAIRE] [PubMed] [DOI]

13.Powell E, Ratnayeke N, Moran NA 2016 Strain diversity and host specificity in a specialized gut symbiont of honey bees and bumble bees. Mol Ecol 25:4461–4471. doi:10.1111/mec.13787.27482856 [OpenAIRE] [PubMed] [DOI]

14.Kwong WK, Moran NA 2016 Gut microbial communities of social bees. Nat Rev Microbiol 14:374–384. doi:10.1038/nrmicro.2016.43.27140688 [OpenAIRE] [PubMed] [DOI]

15.Zheng H, Powell JE, Steele MI, Dietrich C, Moran NA 2017 Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proc Natl Acad Sci U S A 114:4775–4780. doi:10.1073/pnas.1701819114.28420790 [OpenAIRE] [PubMed] [DOI]

74 references, page 1 of 5
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