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

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

doi:10.1371/journal.pone.0027909

Cited by 169 publications

(169 citation statements)

References 116 publications

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“…In other entomopathogenic bacteria, T6SS seem to play a role in the insect infection process (71). Furthermore, T6SS are generally known to function as a virulence factor for many pathogens that interact with eukaryotic cells, including Vibrio cholerae, Pseudomonas aeruginosa, and Burkholderia mallei (72).…”

Section: Resultsmentioning

confidence: 99%

Elucidation of the Photorhabdus temperata Genome and Generation of a Transposon Mutant Library To Identify Motility Mutants Altered in Pathogenesis

Hurst¹,

Rowedder²,

Michaels³

et al. 2015

J. Bacteriol.

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The entomopathogenic nematode Heterorhabditis bacteriophora forms a specific mutualistic association with its bacterial partner Photorhabdus temperata. The microbial symbiont is required for nematode growth and development, and symbiont recognition is strain specific. The aim of this study was to sequence the genome of P. temperata and identify genes that plays a role in the pathogenesis of the Photorhabdus-Heterorhabditis symbiosis. A draft genome sequence of P. temperata strain NC19 was generated. The 5.2-Mb genome was organized into 17 scaffolds and contained 4,808 coding sequences (CDS). A genetic approach was also pursued to identify mutants with altered motility. A bank of 10,000 P. temperata transposon mutants was generated and screened for altered motility patterns. Five classes of motility mutants were identified: (i) nonmotile mutants, (ii) mutants with defective or aberrant swimming motility, (iii) mutant swimmers that do not require NaCl or KCl, (iv) hyperswimmer mutants that swim at an accelerated rate, and (v) hyperswarmer mutants that are able to swarm on the surface of 1.25% agar. The transposon insertion sites for these mutants were identified and used to investigate other physiological properties, including insect pathogenesis. The motility-defective mutant P13-7 had an insertion in the RNase II gene and showed reduced virulence and production of extracellular factors. Genetic complementation of this mutant restored wild-type activity. These results demonstrate a role for RNA turnover in insect pathogenesis and other physiological functions. IMPORTANCEThe relationship between Photorhabdus and entomopathogenic nematode Heterorhabditis represents a well-known mutualistic system that has potential as a biological control agent. The elucidation of the genome of the bacterial partner and role that RNase II plays in its life cycle has provided a greater understanding of Photorhabdus as both an insect pathogen and a nematode symbiont.

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Section: Resultsmentioning

confidence: 99%

Elucidation of the Photorhabdus temperata Genome and Generation of a Transposon Mutant Library To Identify Motility Mutants Altered in Pathogenesis

Hurst¹,

Rowedder²,

Michaels³

et al. 2015

J. Bacteriol.

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“…To create low-and high-Lrp-expressing X. nematophila strains, pMYC4 (low-lrp donor plasmid) and pMYC5 (high-lrp donor plasmid) were inserted into the kefA gene of an lrp-2::kan mutant via biparental conjugation and homologous recombination, respectively. Plasmid integration at the kefA gene locus does not interfere with nematode colonization (4,16,56,57). The Lrp-dependent fluorescence reporter pMYC1 (PfliC-gfp/P lac -rfp) was introduced into the attTn7 site of the genomes in both of the low-Lrp-and high-Lrp-expressing X. nematophila strains described above by triparental conjugation and Tn7 transposition (58,59), creating low-lrp in-genome (low-lrp/Tn7-PfliC-gfp/P lac -rfp) and high-lrp in-genome (high-lrp/Tn7-PfliC-gfp/P lac -rfp) strains.…”

Section: Methodsmentioning

confidence: 99%

High Levels of the Xenorhabdus nematophila Transcription Factor Lrp Promote Mutualism with the Steinernema carpocapsae Nematode Host

Cao

Patel

Rickman

et al. 2017

Appl Environ Microbiol

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Xenorhabdus nematophila bacteria are mutualistic symbionts of Steinernema carpocapsae nematodes and pathogens of insects. The X. nematophila global regulator Lrp controls the expression of many genes involved in both mutualism and pathogenic activities, suggesting a role in the transition between the two host organisms. We previously reported that natural populations of X. nematophila exhibit various levels of Lrp expression and that cells expressing relatively low levels of Lrp are optimized for virulence in the insect Manduca sexta. The adaptive advantage of the high-Lrp-expressing state was not established. Here we used strains engineered to express constitutively high or low levels of Lrp to test the model in which highLrp-expressing cells are adapted for mutualistic activities with the nematode host. We demonstrate that high-Lrp cells form more robust biofilms in laboratory media than do low-Lrp cells, which may reflect adherence to host tissues. Also, our data showed that nematodes cultivated with high-Lrp strains are more frequently colonized than are those associated with low-Lrp strains. Taken together, these data support the idea that high-Lrp cells have an advantage in tissue adherence and colonization initiation. Furthermore, our data show that high-Lrp-expressing strains better support nematode reproduction than do their low-Lrp counterparts under both in vitro and in vivo conditions. Our data indicate that heterogeneity of Lrp expression in X. nematophila populations provides diverse cell populations adapted to both pathogenic (low-Lrp) and mutualistic (high-Lrp) states.IMPORTANCE Host-associated bacteria experience fluctuating conditions during both residence within an individual host and transmission between hosts. For bacteria that engage in evolutionarily stable, long-term relationships with particular hosts, these fluctuations provide selective pressure for the emergence of adaptive regulatory mechanisms. Here we present evidence that the bacterium Xenorhabdus nematophila uses various levels of the transcription factor Lrp to optimize its association with its two animal hosts, nematodes and insects, with which it behaves as a mutualist and a pathogen, respectively. Building on our previous finding that relatively low cellular levels of Lrp are optimal for pathogenesis, we demonstrate that, conversely, high levels of Lrp promote mutualistic activities with the Steinernema carpocapsae nematode host. These data suggest that X. nematophila has evolved to utilize phenotypic variation between high-and low-Lrp-expression states to optimize its alternating behaviors as a mutualist and a pathogen.KEYWORDS virulence modulation, phenotypic variation, symbiosis, colonization initiation

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“…However, a group of genes were identified that showed homology to proteins found in Photorhabdus and/or Xenorhabdus species (Fig. 2B), which are predominantly insect pathogens that associate with nematode vectors (43). These genes included several toxin complex (Tc) gene clusters (Fig.…”

Section: Photorhabdus/ Xenorhabdusmentioning

confidence: 99%

Lack of Overt Genome Reduction in the Bryostatin-Producing Bryozoan Symbiont “Candidatus Endobugula sertula”

Miller

Vanee

Fong

et al. 2016

Appl Environ Microbiol

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The uncultured bacterial symbiont "Candidatus Endobugula sertula" is known to produce cytotoxic compounds called bryostatins, which protect the larvae of its host, Bugula neritina. The symbiont has never been successfully cultured, and it was thought that its genome might be significantly reduced. Here, we took a shotgun metagenomics and metatranscriptomics approach to assemble and characterize the genome of "Ca. Endobugula sertula." We found that it had specific metabolic deficiencies in the biosynthesis of certain amino acids but few other signs of genome degradation, such as small size, abundant pseudogenes, and low coding density. We also identified homologs to genes associated with insect pathogenesis in other gammaproteobacteria, and these genes may be involved in host-symbiont interactions and vertical transmission. Metatranscriptomics revealed that these genes were highly expressed in a reproductive host, along with bry genes for the biosynthesis of bryostatins. We identified two new putative bry genes fragmented from the main bry operon, accounting for previously missing enzymatic functions in the pathway. We also determined that a gene previously assigned to the pathway, bryS, is not expressed in reproductive tissue, suggesting that it is not involved in the production of bryostatins. Our findings suggest that "Ca. Endobugula sertula" may be able to live outside the host if its metabolic deficiencies are alleviated by medium components, which is consistent with recent findings that it may be possible for "Ca. Endobugula sertula" to be transmitted horizontally. IMPORTANCEThe bryostatins are potent protein kinase C activators that have been evaluated in clinical trials for a number of indications, including cancer and Alzheimer's disease. There is, therefore, considerable interest in securing a renewable supply of these compounds, which is currently only possible through aquaculture of Bugula neritina and total chemical synthesis. However, these approaches are labor-intensive and low-yielding and thus preclude the use of bryostatins as a viable therapeutic agent. Our genome assembly and transcriptome analysis for "Ca. Endobugula sertula" shed light on the metabolism of this symbiont, potentially aiding isolation and culturing efforts. Our identification of additional bry genes may also facilitate efforts to express the complete pathway heterologously. Marine invertebrates, such as tunicates and sponges, are known to harbor symbiotic communities of bacteria. Because these animals are sessile and have limited physical defenses, their microbiomes are thought to serve defensive functions, and bacterial symbionts in these invertebrates have been implicated in the production of many bioactive small molecules (1, 2). Such small molecules can possess therapeutically relevant activities, so there is great interest in studying the biosynthetic potential and symbiotic functions of these defensive microorganisms (1, 2). However, most symbionts (and most environmental bacteria in general [1,3,4]) are difficul...

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

Cited by 169 publications

References 116 publications

Elucidation of the Photorhabdus temperata Genome and Generation of a Transposon Mutant Library To Identify Motility Mutants Altered in Pathogenesis

Elucidation of the Photorhabdus temperata Genome and Generation of a Transposon Mutant Library To Identify Motility Mutants Altered in Pathogenesis

High Levels of the Xenorhabdus nematophila Transcription Factor Lrp Promote Mutualism with the Steinernema carpocapsae Nematode Host

Lack of Overt Genome Reduction in the Bryostatin-Producing Bryozoan Symbiont “Candidatus Endobugula sertula”

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