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Attenuated Virulence and Genomic Reductive Evolution in The Attenuated virulence and genomic reductive evolution in the entomopathogenic bacterial symbiont species, Xenorhabdus poinarii Jean-Claude Ogier, Sylvie Pages, Gaelle Bisch, Helene Chiapello, Claudine Médigue, Zoé Rouy, Corinne Teyssier, Stéphanie Vincent, Patrick Tailliez, Alain Givaudan, et al. To cite this version: Jean-Claude Ogier, Sylvie Pages, Gaelle Bisch, Helene Chiapello, Claudine Médigue, et al.. Attenu- ated virulence and genomic reductive evolution in the entomopathogenic bacterial symbiont species, Xenorhabdus poinarii. Genome Biology and Evolution, Society for Molecular Biology and Evolution, 2014, 6, pp.1495-1513. 10.1093/gbe/evu119. hal-01837258 HAL Id: hal-01837258 https://hal.archives-ouvertes.fr/hal-01837258 Submitted on 28 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. GBE Attenuated Virulence and Genomic Reductive Evolution in the Entomopathogenic Bacterial Symbiont Species, Xenorhabdus poinarii Jean-Claude Ogier1,2, Sylvie Page`s1,2,Gae¨lle Bisch1,2,He´le`ne Chiapello3, Claudine Me´digue4,Zoe´ Rouy4, Corinne Teyssier5,Ste´phanie Vincent4, Patrick Tailliez1,2, Alain Givaudan1,2, and Sophie Gaudriault1,2,* 1INRA, UMR Diversite´,Ge´nomes et Interactions Microorganismes-Insectes (DGIMI), Montpellier, France 2Universite´ Montpellier 2, UMR Diversite´,Ge´nomes et Interactions Microorganismes-Insectes (DGIMI), France 3INRA Toulouse Midi-Pyre´ne´es, Unite´ MIA-T, Chemin de Borde Rouge, Castanet-Tolosan, France 4CEA, Genoscope & CNRS, UMR 8030, Laboratoire d’Analyse Bioinformatique en Ge´nomique et Me´tabolisme, Evry, France 5Universite´ Montpellier 1, UFR des Sciences Pharmaceutiques et Biologiques/UMR95 Qualisud, CIRAD-Persyst, France *Corresponding author: E-mail: [email protected]. Downloaded from Accepted: May 30, 2014 Data deposition: This project has been deposited at EBI-ENA under the accession numbers PRJEB4254 and PRJEB4255. Abstract http://gbe.oxfordjournals.org/ Bacteria of the genus Xenorhabdus are symbionts of soil entomopathogenic nematodes of the genus Steinernema. This symbiotic association constitutes an insecticidal complex active against a wide range of insect pests. Unlike other Xenorhabdus species, Xenorhabdus poinarii is avirulent when injected into insects in the absence of its nematode host. We sequenced the genome of the X. poinarii strain G6 and the closely related but virulent X. doucetiae strain FRM16. G6 had a smaller genome (500–700 kb smaller) than virulent Xenorhabdus strains and lacked genes encoding potential virulence factors (hemolysins, type 5 secretion systems, enzymes involved in the synthesis of secondary metabolites, and toxin–antitoxin sys- tems). The genomes of all the X. poinarii strains analyzed here had a similar small size. We did not observe the accumulation of at IFR56 on July 25, 2014 pseudogenes, insertion sequences or decrease in coding density usually seen as a sign of genomic erosion driven by genetic drift in host-adapted bacteria. Instead, genome reduction of X. poinarii seems to have been mediated by the excision of genomic blocks from the flexible genome, as reported for the genomes of attenuated free pathogenic bacteria and some facultative mutualistic bacteria growing exclusively within hosts. This evolutionary pathway probably reflects the adaptation of X. poinarii to specific host. Key words: entomopathogenic bacteria, Lepidoptera, Steinernema, comparative genomics, regions of genomic plasticity, genomic deletion. Introduction interaction (Hussa and Goodrich-Blair 2013). In the Symbioses between microorganisms and animals are wide- Steinernema–Xenorhabdus symbiotic interaction, soil ento- spread in numerous ecological niches. Mutualistic symbiosis mopathogenic nematodes from the genus Steinernema are is based on mutual exploitation, in which each organism con- dependent on their intestinal bacterial symbiont, tributes to the interaction but receives a net positive benefit. Xenorhabdus (Enterobacteriaceae), for colonization of the in- The benefits are diverse and include a mutual influence on sects serving as their nutritional and reproductive niche. A nutrition, defense, reproduction, and development (Chaston nonfeeding soil-dwelling infective juvenile stage of the nem- and Goodrich-Blair 2010). Multipartite microbial symbiosis in- atode penetrates the hemocel of the insect and releases the volves long-term associations between three or more species, bacteria into the hemolymph. The bacterial symbiont helps to with at least two of the partners benefiting from the overcome insect immunity, kills the insect, and converts the ß The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Genome Biol. Evol. 6(6):1495–1513. doi:10.1093/gbe/evu119 Advance Access publication June 5, 2014 1495 Ogieretal. GBE cadaver into an essential source of food for nematode growth difficult to evaluate the facultative status of the St. glaseri–X. and development. Nematodes undergo several rounds of re- poinarii association. production within the insect cadaver. When nematode density Host-adapted bacteria have been described in both mutu- becomes too high and the nutrients derived from the cadaver alistic and pathogenic symbioses. Obligatory mutualistic sym- are exhausted, the bacteria recolonize the nematodes, which bionts of insects (e.g., Buchnera, Wigglesworthia, etc.) live in then emerge from the insect cadaver into the soil, to search specialized host organs (bacteriomes) and share a long-stand- for a new host (Goodrich-Blair and Clarke 2007; Richards and ing coevolutionary history with their host. They are vertically Goodrich-Blair 2009; Nielsen-LeRoux et al. 2012). No free- transmitted and display extreme genomic reduction. living forms of Xenorhabdus have ever been isolated outside Facultative mutualistic symbionts are not strictly necessary of the nematode host (Forst et al. 1997). Except the direct for their host. They do not live exclusively in a specialized vectorization in the insect hemolymph, the benefit of the as- organ and undergo horizontal transfers between host strains sociation to the bacterium has yet to be elucidated. or species (Dale and Moran 2006). These symbionts may be Since the 1980s, various species of entomopathogenic found in an active free-living stage (e.g., the squid symbiont nematodes have been sold and used as effective biological Vibrio fischeri) or may grow exclusively within the hosts (e.g., control. agents for soil-inhabiting insects. Field and laboratory the insect symbiont Wolbachia). Wolbachia,likesomehost- studies have demonstrated the importance of matching the adapted pathogenic bacterial species, such as Burkholderia Downloaded from appropriate nematode species with the particular pest tar- mallei and Mycobacterium leprae, displays a massive expan- geted (Ehlers 2001). For example, the Steinernema sion of insertion sequences (IS), leading to pseudogene forma- carpocapsae–Xenorhabdus nematophila couple is virulent in tion, chromosomal rearrangements mediated by various insect orders, and has been shown to be effective recombination between IS and moderate genome downsiz- against Pseudaletia unipuncta (Lepidoptera), Acheta domesti- ing. These features are considered to constitute the initial http://gbe.oxfordjournals.org/ cus (Orthoptera), and Plectrodera scalator (Coleoptera). By stages of a drastic reduction of genome size (Moran and contrast, the St. glaseri–Xenorhabdus poinarii couple is viru- Plague 2004; Gomez-Valero et al. 2007; Song et al. 2010). lent principally in a few coleopteran species, such as Popillia Finally, some host-adapted pathogenic bacteria, such as My. japonica and Cyclocephala hirta, suggesting a potentially tuberculosis and the asymptomatic bacteriuria (ABU) strains of narrow host specificity (Wang et al. 1994; Converse and Escherichia coli, display moderate genome downsizing with- Grewal 1998; Rosa et al. 2002; Fallon et al. 2006). out massive IS expansion (Zdziarski et al. 2008; Veyrieretal. Co-operation between the bacterial and the helminthic 2011). In such cases, the decrease in genome size probably partner also differs between entomopathogenic couples. results from the excision of mobile genetic elements. at IFR56 on July 25, 2014 Under laboratory conditions, the bacterium or the nematode We focused here on the pathogenic and genomic proper- can be entomopathogenic alone. The injection of a dose of ties of the very poorly documented species X. poinarii.We 100 cells of the bacteria X. nematophila and X. bovienii into compared the virulence of five X. poinarii strains by injecting larvae is lethal in diverse insects (Poinar and Thomas 1966; them into the lepidopteran Spodoptera littoralis.Wecon- Forstetal.1997; Ansari et al. 2003; Sugaretal.2012). firmed that all five
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