Xenorhabdus bovienii Strain Diversity Impacts Coevolution and Symbiotic Maintenance with Steinernema spp. Nematode Hosts
Abstract
Microbial symbionts provide benefits that contribute to the ecology and fitness of host plants and animals. Therefore, the evolutionary success of plants and animals fundamentally depends on long-term maintenance of beneficial associations. Most work investigating coevolution and symbiotic maintenance has focused on species-level associations, and studies are lacking that assess the impact of bacterial strain diversity on symbiotic associations within a coevolutionary framework. Here, we demonstrate that fitness in mutualism varies depending on bacterial strain identity, and this is consistent with variation shaping phylogenetic patterns and maintenance through fitness benefits. Through genome sequencing of nine bacterial symbiont strains and cophylogenetic analysis, we demonstrate diversity among Xenorhabdus bovienii bacteria. Further, we identified cocladogenesis between Steinernema feltiae nematode hosts and their corresponding X. bovienii symbiont strains, indicating potential specificity within the association. To test the specificity, we performed laboratory crosses of nematode hosts with native and nonnative symbiont strains, which revealed that combinations with the native bacterial symbiont and closely related strains performed significantly better than those with more divergent symbionts. Through genomic analyses we also defined potential factors contributing to specificity between nematode hosts and bacterial symbionts. These results suggest that strain-level diversity (e.g., subspecies-level differences) in microbial symbionts can drive variationmore »
- Authors:
-
- Univ. of Wisconsin, Madison, WI (United States)
- Univ. of Arizona, Tucson, AZ (United States)
- Univ. of Wisconsin, Milwaukee, WI (United States)
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Science Foundation (NSF); National Institutes of Health (NIH) National Research Service; National Science and Engineering Research Council of Canada (NSERC Canada)
- OSTI Identifier:
- 1626082
- Grant/Contract Number:
- FC02-07ER64494; IOS-0920631; IOS-0919912; IOS-0919565; T32AI55397; T32 GM07215
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Name: mBio (Online); Journal Volume: 6; Journal Issue: 3; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology (ASM)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Microbiology
Citation Formats
Murfin, Kristen E., Lee, Ming-Min, Klassen, Jonathan L., McDonald, Bradon R., Larget, Bret, Forst, Steven, Stock, S. Patricia, Currie, Cameron R., and Goodrich-Blair, Heidi. Xenorhabdus bovienii Strain Diversity Impacts Coevolution and Symbiotic Maintenance with Steinernema spp. Nematode Hosts. United States: N. p., 2015.
Web. doi:10.1128/mbio.00076-15.
Murfin, Kristen E., Lee, Ming-Min, Klassen, Jonathan L., McDonald, Bradon R., Larget, Bret, Forst, Steven, Stock, S. Patricia, Currie, Cameron R., & Goodrich-Blair, Heidi. Xenorhabdus bovienii Strain Diversity Impacts Coevolution and Symbiotic Maintenance with Steinernema spp. Nematode Hosts. United States. https://doi.org/10.1128/mbio.00076-15
Murfin, Kristen E., Lee, Ming-Min, Klassen, Jonathan L., McDonald, Bradon R., Larget, Bret, Forst, Steven, Stock, S. Patricia, Currie, Cameron R., and Goodrich-Blair, Heidi. Thu .
"Xenorhabdus bovienii Strain Diversity Impacts Coevolution and Symbiotic Maintenance with Steinernema spp. Nematode Hosts". United States. https://doi.org/10.1128/mbio.00076-15. https://www.osti.gov/servlets/purl/1626082.
@article{osti_1626082,
title = {Xenorhabdus bovienii Strain Diversity Impacts Coevolution and Symbiotic Maintenance with Steinernema spp. Nematode Hosts},
author = {Murfin, Kristen E. and Lee, Ming-Min and Klassen, Jonathan L. and McDonald, Bradon R. and Larget, Bret and Forst, Steven and Stock, S. Patricia and Currie, Cameron R. and Goodrich-Blair, Heidi},
abstractNote = {Microbial symbionts provide benefits that contribute to the ecology and fitness of host plants and animals. Therefore, the evolutionary success of plants and animals fundamentally depends on long-term maintenance of beneficial associations. Most work investigating coevolution and symbiotic maintenance has focused on species-level associations, and studies are lacking that assess the impact of bacterial strain diversity on symbiotic associations within a coevolutionary framework. Here, we demonstrate that fitness in mutualism varies depending on bacterial strain identity, and this is consistent with variation shaping phylogenetic patterns and maintenance through fitness benefits. Through genome sequencing of nine bacterial symbiont strains and cophylogenetic analysis, we demonstrate diversity among Xenorhabdus bovienii bacteria. Further, we identified cocladogenesis between Steinernema feltiae nematode hosts and their corresponding X. bovienii symbiont strains, indicating potential specificity within the association. To test the specificity, we performed laboratory crosses of nematode hosts with native and nonnative symbiont strains, which revealed that combinations with the native bacterial symbiont and closely related strains performed significantly better than those with more divergent symbionts. Through genomic analyses we also defined potential factors contributing to specificity between nematode hosts and bacterial symbionts. These results suggest that strain-level diversity (e.g., subspecies-level differences) in microbial symbionts can drive variation in the success of host-microbe associations, and this suggests that these differences in symbiotic success could contribute to maintenance of the symbiosis over an evolutionary time scale.},
doi = {10.1128/mbio.00076-15},
journal = {mBio (Online)},
number = 3,
volume = 6,
place = {United States},
year = {Thu Jun 04 00:00:00 EDT 2015},
month = {Thu Jun 04 00:00:00 EDT 2015}
}
Web of Science
Works referenced in this record:
Shiga Toxin Pathogenesis: Kidney Complications and Renal Failure
book, January 2011
- Obrig, Tom G.; Karpman, Diana
- Current Topics in Microbiology and Immunology
Proteomic Identification of a Novel Toxin Protein (Txp40) from Xenorhabdus nematophila and Its Insecticidal Activity against Larvae of Plutella xylostella
journal, April 2012
- Park, Jae-Min; Kim, Mina; Min, Jiho
- Journal of Agricultural and Food Chemistry, Vol. 60, Issue 16
A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory: Peptide synthetase protects symbiotum
journal, July 2005
- Tanaka, Aiko; Tapper, Brian A.; Popay, Alison
- Molecular Microbiology, Vol. 57, Issue 4
On the Genetic Architecture of Cytoplasmic Incompatibility: Inference from Phenotypic Data
journal, July 2013
- Nor, Igor; Engelstädter, Jan; Duron, Olivier
- The American Naturalist, Vol. 182, Issue 1
The Entomopathogenic Bacterial Endosymbionts Xenorhabdus and Photorhabdus: Convergent Lifestyles from Divergent Genomes
journal, November 2011
- Chaston, John M.; Suen, Garret; Tucker, Sarah L.
- PLoS ONE, Vol. 6, Issue 11
Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture
journal, July 2009
- Berg, Gabriele
- Applied Microbiology and Biotechnology, Vol. 84, Issue 1
MicroScope—an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data
journal, November 2012
- Vallenet, David; Belda, Eugeni; Calteau, Alexandra
- Nucleic Acids Research, Vol. 41, Issue D1
PAML: a program package for phylogenetic analysis by maximum likelihood
journal, January 1997
- Yang, Ziheng
- Bioinformatics, Vol. 13, Issue 5
Symbiotic Effectiveness of Rhizobial Mutualists Varies in Interactions with Native Australian Legume Genera
journal, August 2011
- Thrall, Peter H.; Laine, Anna-Liisa; Broadhurst, Linda M.
- PLoS ONE, Vol. 6, Issue 8
Animals in a bacterial world, a new imperative for the life sciences
journal, February 2013
- McFall-Ngai, Margaret; Hadfield, Michael G.; Bosch, Thomas C. G.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 9
Facultative bacterial symbionts in aphids confer resistance to parasitic wasps
journal, January 2003
- Oliver, K. M.; Russell, J. A.; Moran, N. A.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 4
Thermal adaptation of entomopathogenic nematodes: Niche breadth for infection, establishment, and reproduction
journal, August 1994
- Grewal, Parwinder S.; Selvan, Sen; Gaugler, Randy
- Journal of Thermal Biology, Vol. 19, Issue 4
Species specificity of symbiosis and secondary metabolism in ascidians
journal, August 2014
- Tianero, Ma Diarey B.; Kwan, Jason C.; Wyche, Thomas P.
- The ISME Journal, Vol. 9, Issue 3
Economic contract theory tests models of mutualism
journal, August 2010
- Weyl, E. G.; Frederickson, M. E.; Yu, D. W.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 36
Role of Symbiotic Auxotrophy in the Rhizobium-Legume Symbioses
journal, November 2010
- Prell, Jurgen; Bourdès, Alexandre; Kumar, Shalini
- PLoS ONE, Vol. 5, Issue 11
Host-Gut Microbiota Metabolic Interactions
journal, June 2012
- Nicholson, J. K.; Holmes, E.; Kinross, J.
- Science, Vol. 336, Issue 6086
Lipopeptides from Bacillus and Paenibacillus spp.: A Gold Mine of Antibiotic Candidates: BACILLUS AND PAENIBACILLUS LIPOPEPTIDES
journal, May 2014
- Cochrane, Stephen A.; Vederas, John C.
- Medicinal Research Reviews, Vol. 36, Issue 1
A multilocus approach to assessing co-evolutionary relationships between Steinernema spp. (Nematoda: Steinernematidae) and their bacterial symbionts Xenorhabdus spp. (γ-Proteobacteria: Enterobacteriaceae)
journal, August 2010
- Lee, Ming-Min; Stock, S. Patricia
- Systematic Parasitology, Vol. 77, Issue 1
Gene-Swapping Mediates Host Specificity among Symbiotic Bacteria in a Beneficial Symbiosis
journal, July 2014
- Chavez-Dozal, Alba A.; Gorman, Clayton; Lostroh, C. Phoebe
- PLoS ONE, Vol. 9, Issue 7
The biosynthetic gene cluster for the polyketide immunosuppressant rapamycin.
journal, August 1995
- Schwecke, T.; Aparicio, J. F.; Molnar, I.
- Proceedings of the National Academy of Sciences, Vol. 92, Issue 17
Effect of native Xenorhabdus on the fitness of their Steinernema hosts: contrasting types of interaction
journal, December 2003
- Sicard, Mathieu; Le Brun, Nathalie; Pages, Sylvie
- Parasitology Research, Vol. 91, Issue 6
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008
- Zerbino, D. R.; Birney, E.
- Genome Research, Vol. 18, Issue 5
Friend and foe: the two faces of Xenorhabdus nematophila
journal, August 2007
- Herbert, Erin E.; Goodrich-Blair, Heidi
- Nature Reviews Microbiology, Vol. 5, Issue 8
Exploring the symbiotic pangenome of the nitrogen-fixing bacterium Sinorhizobium meliloti
journal, May 2011
- Galardini, Marco; Mengoni, Alessio; Brilli, Matteo
- BMC Genomics, Vol. 12, Issue 1
Phenotypic variation and host interactions of Xenorhabdus bovienii SS-2004, the entomopathogenic symbiont of Steinernema jollieti nematodes: Xenorhabdus bovienii host interactions
journal, December 2011
- Sugar, Darby R.; Murfin, Kristen E.; Chaston, John M.
- Environmental Microbiology, Vol. 14, Issue 4
The Number of Evolutionary Trees
journal, March 1978
- Felsenstein, Joseph
- Systematic Zoology, Vol. 27, Issue 1
Elucidation of sevadicin, a novel non-ribosomal peptide secondary metabolite produced by the honey bee pathogenic bacterium P aenibacillus larvae: Sevadicin, a non-ribosomal peptide produced by P. larvae
journal, March 2014
- Garcia-Gonzalez, Eva; Müller, Sebastian; Ensle, Paul
- Environmental Microbiology, Vol. 16, Issue 5
Toxicity of Irradiated Media for Xenorhabdus spp
journal, January 1990
- Xu, Jimin; Hurlbert, Ronald E.
- Applied and Environmental Microbiology, Vol. 56, Issue 3
Strong contributors to network persistence are the most vulnerable to extinction
journal, September 2011
- Saavedra, Serguei; Stouffer, Daniel B.; Uzzi, Brian
- Nature, Vol. 478, Issue 7368
Phylogenetic Analysis of Protein Sequence Data Using the Randomized Axelerated Maximum Likelihood ( RAXML ) Program
journal, October 2011
- Rokas, Antonis
- Current Protocols in Molecular Biology, Vol. 96, Issue 1
Techniques in insect nematology
book, January 1997
- Kaya, Harry K.; Stock, S. Patricia
- Manual of Techniques in Insect Pathology
Pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii, studied in twins
journal, February 2011
- Hansen, E. E.; Lozupone, C. A.; Rey, F. E.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009
- Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T.
- Bioinformatics, Vol. 25, Issue 15
The Hologenomic Basis of Speciation: Gut Bacteria Cause Hybrid Lethality in the Genus Nasonia
journal, July 2013
- Brucker, R. M.; Bordenstein, S. R.
- Science, Vol. 341, Issue 6146
Using the Velvet de novo Assembler for Short‐Read Sequencing Technologies
journal, September 2010
- Zerbino, Daniel R.
- Current Protocols in Bioinformatics, Vol. 31, Issue 1
jModelTest: Phylogenetic Model Averaging
journal, April 2008
- Posada, D.
- Molecular Biology and Evolution, Vol. 25, Issue 7
Diet Drives Convergence in Gut Microbiome Functions Across Mammalian Phylogeny and Within Humans
journal, May 2011
- Muegge, B. D.; Kuczynski, J.; Knights, D.
- Science, Vol. 332, Issue 6032
MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004
- Edgar, Robert C.
- BMC Bioinformatics, Vol. 5, Issue 1, p. 113
Intergenomic Epistasis and Coevolutionary Constraint in Plants and Rhizobia
journal, January 2010
- Heath, Katy D.
- Evolution
ORFcor: Identifying and Accommodating ORF Prediction Inconsistencies for Phylogenetic Analysis
journal, March 2013
- Klassen, Jonathan L.; Currie, Cameron R.
- PLoS ONE, Vol. 8, Issue 3
Phylogenetic relationships of Steinernema Travassos, 1927 (Nematoda: Cephalobina: Steinernematidae) based on nuclear, mitochondrial and morphological data
journal, March 2006
- Nadler, Steven A.; Bolotin, Eugene; Stock, S. Patricia
- Systematic Parasitology, Vol. 63, Issue 3
MaGe: a microbial genome annotation system supported by synteny results
journal, January 2006
- Vallenet, D.
- Nucleic Acids Research, Vol. 34, Issue 1
Detection of Influential Observation in Linear Regression
journal, February 1977
- Cook, R. Dennis
- Technometrics, Vol. 19, Issue 1
Infective juvenile formation in the insect parasitic nematode Steinernema feltiae
journal, August 1989
- Popiel, Irene; Grove, Donna L.; Friedman, M. J.
- Parasitology, Vol. 99, Issue 1
MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
- Edgar, R. C.
- Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
Genomic insights that advance the species definition for prokaryotes
journal, February 2005
- Konstantinidis, K. T.; Tiedje, J. M.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 7
The Steinernema carpocapsae intestinal vesicle contains a subcellular structure with which Xenorhabdus nematophila associates during colonization initiation
journal, December 2005
- Martens, Eric C.; Goodrich-Blair, Heidi
- Cellular Microbiology, Vol. 7, Issue 12
MrBayes 3: Bayesian phylogenetic inference under mixed models
journal, August 2003
- Ronquist, Fredrik; Huelsenbeck, John P.
- Bioinformatics, Vol. 19, Issue 12, p. 1572-1574
Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy
journal, April 2011
- Letunic, I.; Bork, P.
- Nucleic Acids Research, Vol. 39, Issue suppl
Pfam: the protein families database
journal, November 2013
- Finn, Robert D.; Bateman, Alex; Clements, Jody
- Nucleic Acids Research, Vol. 42, Issue D1
Evolutionary Perspectives in a Mutualism of Sepiolid Squid and Bioluminescent Bacteria: Combined Usage of Microbial Experimental Evolution and Temporal Population Genetics: Evolutionary Perspectives in a Mutualism of Sepiolid Squid and Bioluminescent Bacteria
journal, January 2012
- Soto, W.; Punke, E. B.; Nishiguchi, M. K.
- Evolution, Vol. 66, Issue 5
A multigene approach for assessing evolutionary relationships of Xenorhabdus spp. (γ-Proteobacteria), the bacterial symbionts of entomopathogenic Steinernema nematodes
journal, June 2010
- Lee, Ming-Min; Stock, S. Patricia
- Journal of Invertebrate Pathology, Vol. 104, Issue 2
Comparisons of dN/dS are time dependent for closely related bacterial genomes
journal, March 2006
- Rocha, Eduardo P. C.; Smith, John Maynard; Hurst, Laurence D.
- Journal of Theoretical Biology, Vol. 239, Issue 2
MAFFT: Iterative Refinement and Additional Methods
book, January 2013
- Katoh, Kazutaka; Standley, Daron M.
- Methods in Molecular Biology
Phylogenetic Analysis of Protein Sequence Data Using the Randomized Axelerated Maximum Likelihood ( RAXML ) Program
journal, October 2011
- Rokas, Antonis
- Current Protocols in Molecular Biology, Vol. 96, Issue 1
MAFFT: Iterative Refinement and Additional Methods
book, January 2013
- Katoh, Kazutaka; Standley, Daron M.
- Methods in Molecular Biology
Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture
journal, July 2009
- Berg, Gabriele
- Applied Microbiology and Biotechnology, Vol. 84, Issue 1
Effect of native Xenorhabdus on the fitness of their Steinernema hosts: contrasting types of interaction
journal, December 2003
- Sicard, Mathieu; Le Brun, Nathalie; Pages, Sylvie
- Parasitology Research, Vol. 91, Issue 6
Molecular and biological characterization of an isolate of the potyvirus passiflora virus Y naturally infecting soybean (Glycine max) in Brazil
journal, September 2022
- Ribeiro-Junior, Marcos Roberto; Barreto da Silva, Felipe; Marubayashi, Julio Massaharu
- Archives of Virology, Vol. 167, Issue 12
Phylogenetic relationships of Steinernema Travassos, 1927 (Nematoda: Cephalobina: Steinernematidae) based on nuclear, mitochondrial and morphological data
journal, March 2006
- Nadler, Steven A.; Bolotin, Eugene; Stock, S. Patricia
- Systematic Parasitology, Vol. 63, Issue 3
Thermal adaptation of entomopathogenic nematodes: Niche breadth for infection, establishment, and reproduction
journal, August 1994
- Grewal, Parwinder S.; Selvan, Sen; Gaugler, Randy
- Journal of Thermal Biology, Vol. 19, Issue 4
A multigene approach for assessing evolutionary relationships of Xenorhabdus spp. (γ-Proteobacteria), the bacterial symbionts of entomopathogenic Steinernema nematodes
journal, June 2010
- Lee, Ming-Min; Stock, S. Patricia
- Journal of Invertebrate Pathology, Vol. 104, Issue 2
Coexistence of two steinernematid nematode species (Rhabditida: Steinernematidae) in the presence of two host species
journal, November 1996
- Koppenhöfer, Albrecht M.; Kaya, Harry K.
- Applied Soil Ecology, Vol. 4, Issue 3
Significance of Achromobacter nematophilus Poinar and Thomas (Achromobacteraceae: Eubacteriales) in the development of the nematode, DD-136 ( Neoaplectana sp. Steinernematidae)
journal, May 1966
- Poinar, George O.; Thomas, Gerard M.
- Parasitology, Vol. 56, Issue 2
Proteomic Identification of a Novel Toxin Protein (Txp40) from Xenorhabdus nematophila and Its Insecticidal Activity against Larvae of Plutella xylostella
journal, April 2012
- Park, Jae-Min; Kim, Mina; Min, Jiho
- Journal of Agricultural and Food Chemistry, Vol. 60, Issue 16
Species specificity of symbiosis and secondary metabolism in ascidians
journal, August 2014
- Tianero, Ma Diarey B.; Kwan, Jason C.; Wyche, Thomas P.
- The ISME Journal, Vol. 9, Issue 3
Strong contributors to network persistence are the most vulnerable to extinction
journal, September 2011
- Saavedra, Serguei; Stouffer, Daniel B.; Uzzi, Brian
- Nature, Vol. 478, Issue 7368
Friend and foe: the two faces of Xenorhabdus nematophila
journal, August 2007
- Herbert, Erin E.; Goodrich-Blair, Heidi
- Nature Reviews Microbiology, Vol. 5, Issue 8
Pneumococcal within-host diversity during colonization, transmission and treatment
journal, October 2022
- Tonkin-Hill, Gerry; Ling, Clare; Chaguza, Chrispin
- Nature Microbiology, Vol. 7, Issue 11
Facultative bacterial symbionts in aphids confer resistance to parasitic wasps
journal, January 2003
- Oliver, K. M.; Russell, J. A.; Moran, N. A.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 4
Genomic insights that advance the species definition for prokaryotes
journal, February 2005
- Konstantinidis, K. T.; Tiedje, J. M.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 7
Economic contract theory tests models of mutualism
journal, August 2010
- Weyl, E. G.; Frederickson, M. E.; Yu, D. W.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 36
Animals in a bacterial world, a new imperative for the life sciences
journal, February 2013
- McFall-Ngai, Margaret; Hadfield, Michael G.; Bosch, Thomas C. G.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 9
The biosynthetic gene cluster for the polyketide immunosuppressant rapamycin.
journal, August 1995
- Schwecke, T.; Aparicio, J. F.; Molnar, I.
- Proceedings of the National Academy of Sciences, Vol. 92, Issue 17
PAML: a program package for phylogenetic analysis by maximum likelihood
journal, January 1997
- Yang, Ziheng
- Bioinformatics, Vol. 13, Issue 5
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009
- Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T.
- Bioinformatics, Vol. 25, Issue 15
jModelTest: Phylogenetic Model Averaging
journal, April 2008
- Posada, D.
- Molecular Biology and Evolution, Vol. 25, Issue 7
Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy
journal, April 2011
- Letunic, I.; Bork, P.
- Nucleic Acids Research, Vol. 39, Issue suppl
MicroScope—an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data
journal, November 2012
- Vallenet, David; Belda, Eugeni; Calteau, Alexandra
- Nucleic Acids Research, Vol. 41, Issue D1
Elucidation of sevadicin, a novel non-ribosomal peptide secondary metabolite produced by the honey bee pathogenic bacterium P aenibacillus larvae: Sevadicin, a non-ribosomal peptide produced by P. larvae
journal, March 2014
- Garcia-Gonzalez, Eva; Müller, Sebastian; Ensle, Paul
- Environmental Microbiology, Vol. 16, Issue 5
A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory: Peptide synthetase protects symbiotum
journal, July 2005
- Tanaka, Aiko; Tapper, Brian A.; Popay, Alison
- Molecular Microbiology, Vol. 57, Issue 4
Phenotypic variation and host interactions of Xenorhabdus bovienii SS-2004, the entomopathogenic symbiont of Steinernema jollieti nematodes: Xenorhabdus bovienii host interactions
journal, December 2011
- Sugar, Darby R.; Murfin, Kristen E.; Chaston, John M.
- Environmental Microbiology, Vol. 14, Issue 4
The Steinernema carpocapsae intestinal vesicle contains a subcellular structure with which Xenorhabdus nematophila associates during colonization initiation
journal, December 2005
- Martens, Eric C.; Goodrich-Blair, Heidi
- Cellular Microbiology, Vol. 7, Issue 12
Intergenomic Epistasis and Coevolutionary Constraint in Plants and Rhizobia
journal, January 2010
- Heath, Katy D.
- Evolution
Evolutionary Perspectives in a Mutualism of Sepiolid Squid and Bioluminescent Bacteria: Combined Usage of Microbial Experimental Evolution and Temporal Population Genetics: Evolutionary Perspectives in a Mutualism of Sepiolid Squid and Bioluminescent Bacteria
journal, January 2012
- Soto, W.; Punke, E. B.; Nishiguchi, M. K.
- Evolution, Vol. 66, Issue 5
Diet Drives Convergence in Gut Microbiome Functions Across Mammalian Phylogeny and Within Humans
journal, May 2011
- Muegge, B. D.; Kuczynski, J.; Knights, D.
- Science, Vol. 332, Issue 6032
Host-Gut Microbiota Metabolic Interactions
journal, June 2012
- Nicholson, J. K.; Holmes, E.; Kinross, J.
- Science, Vol. 336, Issue 6086
The Hologenomic Basis of Speciation: Gut Bacteria Cause Hybrid Lethality in the Genus Nasonia
journal, July 2013
- Brucker, R. M.; Bordenstein, S. R.
- Science, Vol. 341, Issue 6146
Microbial Population Dynamics in the Hemolymph of Manduca sexta Infected with Xenorhabdus nematophila and the Entomopathogenic Nematode Steinernema carpocapsae
journal, May 2014
- Singh, Swati; Reese, Jordan M.; Casanova-Torres, Ángel M.
- Applied and Environmental Microbiology, Vol. 80, Issue 14
Examination of Xenorhabdus nematophila Lipases in Pathogenic and Mutualistic Host Interactions Reveals a Role for xlpA in Nematode Progeny Production
journal, October 2009
- Richards, Gregory R.; Goodrich-Blair, Heidi
- Applied and Environmental Microbiology, Vol. 76, Issue 1
Nonribosomal Peptide Synthase Gene Clusters for Lipopeptide Biosynthesis in Bacillus subtilis 916 and Their Phenotypic Functions
journal, October 2014
- Luo, Chuping; Liu, Xuehui; Zhou, Huafei
- Applied and Environmental Microbiology, Vol. 81, Issue 1
Toxicity of Irradiated Media for Xenorhabdus spp
journal, January 1990
- Xu, Jimin; Hurlbert, Ronald E.
- Applied and Environmental Microbiology, Vol. 56, Issue 3
Competitive Dominance among Strains of Luminous Bacteria Provides an Unusual Form of Evidence for Parallel Evolution in Sepiolid Squid-Vibrio Symbioses
journal, September 1998
- Nishiguchi, Michele K.; Ruby, Edward G.; McFall-Ngai, Margaret J.
- Applied and Environmental Microbiology, Vol. 64, Issue 9
Identification and Functional Characterization of a Xenorhabdus nematophila Oligopeptide Permease
journal, September 2004
- Orchard, Samantha S.; Goodrich-Blair, Heidi
- Applied and Environmental Microbiology, Vol. 70, Issue 9
The xnp1 P2-Like Tail Synthesis Gene Cluster Encodes Xenorhabdicin and Is Required for Interspecies Competition
journal, May 2011
- Morales-Soto, N.; Forst, S. A.
- Journal of Bacteriology, Vol. 193, Issue 14
Early Colonization Events in the Mutualistic Association between Steinernema carpocapsae Nematodes and Xenorhabdus nematophila Bacteria
journal, May 2003
- Martens, Eric C.; Heungens, Kurt; Goodrich-Blair, Heidi
- Journal of Bacteriology, Vol. 185, Issue 10
Analysis of the PixA Inclusion Body Protein of Xenorhabdus nematophila
journal, April 2006
- Goetsch, M.; Owen, H.; Goldman, B.
- Journal of Bacteriology, Vol. 188, Issue 7
MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004
- Edgar, Robert C.
- BMC Bioinformatics, Vol. 5, Issue 1, p. 113
Exploring the symbiotic pangenome of the nitrogen-fixing bacterium Sinorhizobium meliloti
journal, May 2011
- Galardini, Marco; Mengoni, Alessio; Brilli, Matteo
- BMC Genomics, Vol. 12, Issue 1
Role of Symbiotic Auxotrophy in the Rhizobium-Legume Symbioses
journal, November 2010
- Prell, Jurgen; Bourdès, Alexandre; Kumar, Shalini
- PLoS ONE, Vol. 5, Issue 11
Symbiotic Effectiveness of Rhizobial Mutualists Varies in Interactions with Native Australian Legume Genera
journal, August 2011
- Thrall, Peter H.; Laine, Anna-Liisa; Broadhurst, Linda M.
- PLoS ONE, Vol. 6, Issue 8
Detection of Influential Observation in Linear Regression
journal, February 1977
- Cook, R. Dennis
- Technometrics, Vol. 19, Issue 1
The Number of Evolutionary Trees
journal, March 1978
- Felsenstein, Joseph
- Systematic Zoology, Vol. 27, Issue 1
Works referencing / citing this record:
Correction: Phylosymbiosis: Relationships and Functional Effects of Microbial Communities across Host Evolutionary History
journal, January 2017
- Brooks, Andrew W.; Kohl, Kevin D.; Brucker, Robert M.
- PLOS Biology, Vol. 15, Issue 1
Profiling the metabolic signals involved in chemical communication between microbes using imaging mass spectrometry
journal, September 2016
- Stasulli, Nikolas M.; Shank, Elizabeth A.
- FEMS Microbiology Reviews, Vol. 40, Issue 6
Comparison of Xenorhabdus bovienii bacterial strain genomes reveals diversity in symbiotic functions
journal, November 2015
- Murfin, Kristen E.; Whooley, Amy C.; Klassen, Jonathan L.
- BMC Genomics, Vol. 16, Issue 1
The effects of Bacillus subtilis on Caenorhabditis elegans fitness after heat stress
journal, February 2019
- Hoang, Kim L.; Gerardo, Nicole M.; Morran, Levi T.
- Ecology and Evolution, Vol. 9, Issue 6
Transmission Success of Entomopathogenic Nematodes Used in Pest Control
journal, June 2018
- Labaude, Sophie; Griffin, Christine
- Insects, Vol. 9, Issue 2
Caenorhabditis elegans as a Model for Microbiome Research
journal, March 2017
- Zhang, Fan; Berg, Maureen; Dierking, Katja
- Frontiers in Microbiology, Vol. 8
The insect pathogenic bacterium Xenorhabdus innexi has attenuated virulence in multiple insect model hosts yet encodes a potent mosquitocidal toxin
journal, December 2017
- Kim, Il-Hwan; Aryal, Sudarshan K.; Aghai, Dariush T.
- BMC Genomics, Vol. 18, Issue 1
Molecular mechanism of the smart attack of pathogenic bacteria on nematodes
journal, May 2020
- Zhang, Lin; Wei, Yuping; Tao, Ye
- Microbial Biotechnology, Vol. 13, Issue 3
Studying the Symbiotic Bacterium Xenorhabdus nematophila in Individual, Living Steinernema carpocapsae Nematodes Using Microfluidic Systems
journal, January 2018
- Stilwell, Matthew D.; Cao, Mengyi; Goodrich-Blair, Heidi
- mSphere, Vol. 3, Issue 1
Profiling the metabolic signals involved in chemical communication between microbes using imaging mass spectrometry
text, January 2016
- M., Stasulli, Nikolas; A., Shank, Elizabeth
- The University of North Carolina at Chapel Hill University Libraries
Evolution and taxonomy of nematode-associated entomopathogenic bacteria of the genera Xenorhabdus and Photorhabdus: an overview
journal, January 2020
- Sajnaga, Ewa; Kazimierczak, Waldemar
- Symbiosis, Vol. 80, Issue 1
Fitness costs of symbiont switching using entomopathogenic nematodes as a model
journal, April 2017
- McMullen, John G.; Peterson, Brittany F.; Forst, Steven
- BMC Evolutionary Biology, Vol. 17, Issue 1
Nematode-bacteria mutualism: Selection within the mutualism supersedes selection outside of the mutualism: BRIEF COMMUNICATION
journal, March 2016
- Morran, Levi T.; Penley, McKenna J.; Byrd, Victoria S.
- Evolution, Vol. 70, Issue 3
The model squid–vibrio symbiosis provides a window into the impact of strain‐ and species‐level differences during the initial stages of symbiont engagement
journal, August 2018
- Koehler, Sabrina; Gaedeke, Roxane; Thompson, Cecilia
- Environmental Microbiology, Vol. 21, Issue 9
Trade-off between reproductive and anti-competitor abilities in an insect-parasitic nematode-bacteria symbiosis
journal, October 2018
- Bertoloni Meli, Sofia; Bashey, Farrah
- Ecology and Evolution, Vol. 8, Issue 22
Comparative Genomics between Two Xenorhabdus bovienii Strains Highlights Differential Evolutionary Scenarios within an Entomopathogenic Bacterial Species
journal, January 2016
- Bisch, Gaëlle; Ogier, Jean-Claude; Médigue, Claudine
- Genome Biology and Evolution, Vol. 8, Issue 1
Phylosymbiosis: Relationships and Functional Effects of Microbial Communities across Host Evolutionary History
journal, November 2016
- Brooks, Andrew W.; Kohl, Kevin D.; Brucker, Robert M.
- PLOS Biology, Vol. 14, Issue 11
An Entomopathogenic Nematode Extends Its Niche by Associating with Different Symbionts
journal, August 2016
- Maher, Abigail M. D.; Asaiyah, Mohamed A. M.; Brophy, Caroline
- Microbial Ecology, Vol. 73, Issue 1
Influence of symbiotic and non-symbiotic bacteria on pheromone production in Steinernema nematodes (Nematoda, Steinernematidae)
journal, September 2019
- Roder, Alexandra C.; Wang, Yuting; Butcher, Rebecca A.
- The Journal of Experimental Biology, Vol. 222, Issue 18
Trade-off between reproductive and anti-competitor abilities in an insect-parasitic nematode-bacteria symbiosis
journal, October 2018
- Bertoloni Meli, Sofia; Bashey, Farrah
- Ecology and Evolution, Vol. 8, Issue 22
Steinernema poinari (Nematoda: Steinernematidae): a new symbiotic host of entomopathogenic bacteria Xenorhabdus bovienii
journal, June 2018
- Sajnaga, Ewa; Kazimierczak, Waldemar; Skowronek, Marcin
- Archives of Microbiology, Vol. 200, Issue 9
Comparative Genomics between Two Xenorhabdus bovienii Strains Highlights Differential Evolutionary Scenarios within an Entomopathogenic Bacterial Species
journal, January 2016
- Bisch, Gaëlle; Ogier, Jean-Claude; Médigue, Claudine
- Genome Biology and Evolution, Vol. 8, Issue 1
Molecular mechanism of the smart attack of pathogenic bacteria on nematodes
journal, May 2020
- Zhang, Lin; Wei, Yuping; Tao, Ye
- Microbial Biotechnology, Vol. 13, Issue 3
Fitness costs of symbiont switching using entomopathogenic nematodes as a model
journal, April 2017
- McMullen, John G.; Peterson, Brittany F.; Forst, Steven
- BMC Evolutionary Biology, Vol. 17, Issue 1
Comparison of Xenorhabdus bovienii bacterial strain genomes reveals diversity in symbiotic functions
journal, November 2015
- Murfin, Kristen E.; Whooley, Amy C.; Klassen, Jonathan L.
- BMC Genomics, Vol. 16, Issue 1
Phylosymbiosis: Relationships and Functional Effects of Microbial Communities across Host Evolutionary History
journal, November 2016
- Brooks, Andrew W.; Kohl, Kevin D.; Brucker, Robert M.
- PLOS Biology, Vol. 14, Issue 11
Caenorhabditis elegans as a Model for Microbiome Research
journal, March 2017
- Zhang, Fan; Berg, Maureen; Dierking, Katja
- Frontiers in Microbiology, Vol. 8
Bacteria of the Genus Xenorhabdus, a Novel Source of Bioactive Compounds
journal, December 2018
- Dreyer, Jönike; Malan, Antoinette P.; Dicks, Leon M. T.
- Frontiers in Microbiology, Vol. 9
Transmission Success of Entomopathogenic Nematodes Used in Pest Control
journal, June 2018
- Labaude, Sophie; Griffin, Christine
- Insects, Vol. 9, Issue 2