The Entomopathogenic Bacterial Endosymbionts Xenorhabdus and Photorhabdus: Convergent Lifestyles from Divergent Genomes

John M. Chaston; Garret Suen; Sarah L. Tucker; Aaron W. Andersen; Archna Bhasin; Edna Bode; Helge B. Bode; Alexander O. Brachmann; Charles E. Cowles; Kimberly N. Cowles; Creg Darby; Limaris de Léon; Kevin Drace; Zijin Du; Alain Givaudan; Erin E. Herbert Tran; Kelsea A. Jewell; Jennifer J. Knack; Karina C. Krasomil-Osterfeld; Ryan Kukor; Anne Lanois; Phil Latreille; Nancy K. Leimgruber; Carolyn M. Lipke; Renyi Liu; Xiaojun Lu; Eric C. Martens; Pradeep R. Marri; Claudine Médigue; Megan L. Menard; Nancy M. Miller; Nydia Morales-Soto; Stacie Norton; Jean Claude Ogier; Samantha S. Orchard; Dongjin Park; Youngjin Park; Barbara A. Qurollo; Darby Renneckar Sugar; Gregory R. Richards; Zoé Rouy; Brad Slominski; Kathryn Slominski; Holly Snyder; Brian C. Tjaden; Ransome van der Hoeven; Roy D. Welch; Cathy Wheeler; Bosong Xiang; Brad Barbazuk; Sophie Gaudriault; Brad Goodner; Steven C. Slater; Steven Forst; Barry S. Goldman; Heidi Goodrich-Blair

doi:10.1371/journal.pone.0027909

The Entomopathogenic Bacterial Endosymbionts Xenorhabdus and Photorhabdus: Convergent Lifestyles from Divergent Genomes

John M. Chaston, Garret Suen, Sarah L. Tucker, Aaron W. Andersen, Archna Bhasin, Edna Bode, Helge B. Bode, Alexander O. Brachmann, Charles E. Cowles, Kimberly N. Cowles, Creg Darby, Limaris de Léon, Kevin Drace, Zijin Du, Alain Givaudan, Erin E. Herbert Tran, Kelsea A. Jewell, Jennifer J. Knack, Karina C. Krasomil-Osterfeld, Ryan KukorAnne Lanois, Phil Latreille, Nancy K. Leimgruber, Carolyn M. Lipke, Renyi Liu, Xiaojun Lu, Eric C. Martens, Pradeep R. Marri, Claudine Médigue, Megan L. Menard, Nancy M. Miller, Nydia Morales-Soto, Stacie Norton, Jean Claude Ogier, Samantha S. Orchard, Dongjin Park, Youngjin Park, Barbara A. Qurollo, Darby Renneckar Sugar, Gregory R. Richards, Zoé Rouy, Brad Slominski, Kathryn Slominski, Holly Snyder, Brian C. Tjaden, Ransome van der Hoeven, Roy D. Welch, Cathy Wheeler, Bosong Xiang, Brad Barbazuk, Sophie Gaudriault, Brad Goodner, Steven C. Slater, Steven Forst, Barry S. Goldman, Heidi Goodrich-Blair

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Abstract

Members of the genus Xenorhabdus are entomopathogenic bacteria that associate with nematodes. The nematode-bacteria pair infects and kills insects, with both partners contributing to insect pathogenesis and the bacteria providing nutrition to the nematode from available insect-derived nutrients. The nematode provides the bacteria with protection from predators, access to nutrients, and a mechanism of dispersal. Members of the bacterial genus Photorhabdus also associate with nematodes to kill insects, and both genera of bacteria provide similar services to their different nematode hosts through unique physiological and metabolic mechanisms. We posited that these differences would be reflected in their respective genomes. To test this, we sequenced to completion the genomes of Xenorhabdus nematophila ATCC 19061 and Xenorhabdus bovienii SS-2004. As expected, both Xenorhabdus genomes encode many anti-insecticidal compounds, commensurate with their entomopathogenic lifestyle. Despite the similarities in lifestyle between Xenorhabdus and Photorhabdus bacteria, a comparative analysis of the Xenorhabdus, Photorhabdus luminescens, and P. asymbiotica genomes suggests genomic divergence. These findings indicate that evolutionary changes shaped by symbiotic interactions can follow different routes to achieve similar end points.

Original language	English (US)
Article number	e27909
Journal	PloS one
Volume	6
Issue number	11
DOIs	https://doi.org/10.1371/journal.pone.0027909
State	Published - 2011

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Chaston, J. M., Suen, G., Tucker, S. L., Andersen, A. W., Bhasin, A., Bode, E., Bode, H. B., Brachmann, A. O., Cowles, C. E., Cowles, K. N., Darby, C., de Léon, L., Drace, K., Du, Z., Givaudan, A., Herbert Tran, E. E., Jewell, K. A., Knack, J. J., Krasomil-Osterfeld, K. C., ... Goodrich-Blair, H. (2011). The Entomopathogenic Bacterial Endosymbionts Xenorhabdus and Photorhabdus: Convergent Lifestyles from Divergent Genomes. PloS one, 6(11), Article e27909. https://doi.org/10.1371/journal.pone.0027909

Chaston, JM, Suen, G, Tucker, SL, Andersen, AW, Bhasin, A, Bode, E, Bode, HB, Brachmann, AO, Cowles, CE, Cowles, KN, Darby, C, de Léon, L, Drace, K, Du, Z, Givaudan, A, Herbert Tran, EE, Jewell, KA, Knack, JJ, Krasomil-Osterfeld, KC, Kukor, R, Lanois, A, Latreille, P, Leimgruber, NK, Lipke, CM, Liu, R, Lu, X, Martens, EC, Marri, PR, Médigue, C, Menard, ML, Miller, NM, Morales-Soto, N, Norton, S, Ogier, JC, Orchard, SS, Park, D, Park, Y, Qurollo, BA, Sugar, DR, Richards, GR, Rouy, Z, Slominski, B, Slominski, K, Snyder, H, Tjaden, BC, van der Hoeven, R, Welch, RD, Wheeler, C, Xiang, B, Barbazuk, B, Gaudriault, S, Goodner, B, Slater, SC, Forst, S, Goldman, BS & Goodrich-Blair, H 2011, 'The Entomopathogenic Bacterial Endosymbionts Xenorhabdus and Photorhabdus: Convergent Lifestyles from Divergent Genomes', PloS one, vol. 6, no. 11, e27909. https://doi.org/10.1371/journal.pone.0027909

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title = "The Entomopathogenic Bacterial Endosymbionts Xenorhabdus and Photorhabdus: Convergent Lifestyles from Divergent Genomes",

abstract = "Members of the genus Xenorhabdus are entomopathogenic bacteria that associate with nematodes. The nematode-bacteria pair infects and kills insects, with both partners contributing to insect pathogenesis and the bacteria providing nutrition to the nematode from available insect-derived nutrients. The nematode provides the bacteria with protection from predators, access to nutrients, and a mechanism of dispersal. Members of the bacterial genus Photorhabdus also associate with nematodes to kill insects, and both genera of bacteria provide similar services to their different nematode hosts through unique physiological and metabolic mechanisms. We posited that these differences would be reflected in their respective genomes. To test this, we sequenced to completion the genomes of Xenorhabdus nematophila ATCC 19061 and Xenorhabdus bovienii SS-2004. As expected, both Xenorhabdus genomes encode many anti-insecticidal compounds, commensurate with their entomopathogenic lifestyle. Despite the similarities in lifestyle between Xenorhabdus and Photorhabdus bacteria, a comparative analysis of the Xenorhabdus, Photorhabdus luminescens, and P. asymbiotica genomes suggests genomic divergence. These findings indicate that evolutionary changes shaped by symbiotic interactions can follow different routes to achieve similar end points.",

author = "Chaston, {John M.} and Garret Suen and Tucker, {Sarah L.} and Andersen, {Aaron W.} and Archna Bhasin and Edna Bode and Bode, {Helge B.} and Brachmann, {Alexander O.} and Cowles, {Charles E.} and Cowles, {Kimberly N.} and Creg Darby and {de L{\'e}on}, Limaris and Kevin Drace and Zijin Du and Alain Givaudan and {Herbert Tran}, {Erin E.} and Jewell, {Kelsea A.} and Knack, {Jennifer J.} and Krasomil-Osterfeld, {Karina C.} and Ryan Kukor and Anne Lanois and Phil Latreille and Leimgruber, {Nancy K.} and Lipke, {Carolyn M.} and Renyi Liu and Xiaojun Lu and Martens, {Eric C.} and Marri, {Pradeep R.} and Claudine M{\'e}digue and Menard, {Megan L.} and Miller, {Nancy M.} and Nydia Morales-Soto and Stacie Norton and Ogier, {Jean Claude} and Orchard, {Samantha S.} and Dongjin Park and Youngjin Park and Qurollo, {Barbara A.} and Sugar, {Darby Renneckar} and Richards, {Gregory R.} and Zo{\'e} Rouy and Brad Slominski and Kathryn Slominski and Holly Snyder and Tjaden, {Brian C.} and {van der Hoeven}, Ransome and Welch, {Roy D.} and Cathy Wheeler and Bosong Xiang and Brad Barbazuk and Sophie Gaudriault and Brad Goodner and Slater, {Steven C.} and Steven Forst and Goldman, {Barry S.} and Heidi Goodrich-Blair",

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T2 - Convergent Lifestyles from Divergent Genomes

AU - Chaston, John M.

AU - Suen, Garret

AU - Tucker, Sarah L.

AU - Andersen, Aaron W.

AU - Bhasin, Archna

AU - Bode, Edna

AU - Bode, Helge B.

AU - Brachmann, Alexander O.

AU - Cowles, Charles E.

AU - Cowles, Kimberly N.

AU - Darby, Creg

AU - de Léon, Limaris

AU - Drace, Kevin

AU - Du, Zijin

AU - Givaudan, Alain

AU - Herbert Tran, Erin E.

AU - Jewell, Kelsea A.

AU - Knack, Jennifer J.

AU - Krasomil-Osterfeld, Karina C.

AU - Kukor, Ryan

AU - Lanois, Anne

AU - Latreille, Phil

AU - Leimgruber, Nancy K.

AU - Lipke, Carolyn M.

AU - Liu, Renyi

AU - Lu, Xiaojun

AU - Martens, Eric C.

AU - Marri, Pradeep R.

AU - Médigue, Claudine

AU - Menard, Megan L.

AU - Miller, Nancy M.

AU - Morales-Soto, Nydia

AU - Norton, Stacie

AU - Ogier, Jean Claude

AU - Orchard, Samantha S.

AU - Park, Dongjin

AU - Park, Youngjin

AU - Qurollo, Barbara A.

AU - Sugar, Darby Renneckar

AU - Richards, Gregory R.

AU - Rouy, Zoé

AU - Slominski, Brad

AU - Slominski, Kathryn

AU - Snyder, Holly

AU - Tjaden, Brian C.

AU - van der Hoeven, Ransome

AU - Welch, Roy D.

AU - Wheeler, Cathy

AU - Xiang, Bosong

AU - Barbazuk, Brad

AU - Gaudriault, Sophie

AU - Goodner, Brad

AU - Slater, Steven C.

AU - Forst, Steven

AU - Goldman, Barry S.

AU - Goodrich-Blair, Heidi

PY - 2011

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The Entomopathogenic Bacterial Endosymbionts Xenorhabdus and Photorhabdus: Convergent Lifestyles from Divergent Genomes

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