Comparative Genomic Analysis Reveals Ecological Differentiation in the Genus Carnobacterium Christelle F

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Comparative Genomic Analysis Reveals Ecological Differentiation in the Genus Carnobacterium Christelle F Comparative genomic analysis reveals ecological differentiation in the genus carnobacterium Christelle F. Iskandar, Frederic Borges, Bernard Taminiau, Georges Daube, Monique Zagorec, Benoit Remenant, Jørgen J. Leisner, Martin A. Hansen, Søren J. Sørensen, Cécile Mangavel, et al. To cite this version: Christelle F. Iskandar, Frederic Borges, Bernard Taminiau, Georges Daube, Monique Zagorec, et al.. Comparative genomic analysis reveals ecological differentiation in the genus carnobacterium. Frontiers in Microbiology, Frontiers Media, 2017, 8, pp.1-14. 10.3389/fmicb.2017.00357. hal-01606737 HAL Id: hal-01606737 https://hal.archives-ouvertes.fr/hal-01606737 Submitted on 26 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. Distributed under a Creative Commons Attribution| 4.0 International License fmicb-08-00357 March 6, 2017 Time: 15:38 # 1 ORIGINAL RESEARCH published: 08 March 2017 doi: 10.3389/fmicb.2017.00357 Comparative Genomic Analysis Reveals Ecological Differentiation in the Genus Carnobacterium Christelle F. Iskandar1, Frédéric Borges1*, Bernard Taminiau2, Georges Daube2, Monique Zagorec3, Benoît Remenant3†, Jørgen J. Leisner4, Martin A. Hansen5, Søren J. Sørensen5, Cécile Mangavel1, Catherine Cailliez-Grimal1 and Anne-Marie Revol-Junelles1 1 Laboratoire d’Ingénierie des Biomolécules, École Nationale Supérieure d’Agronomie et des Industries Alimentaires – Université de Lorraine, Vandoeuvre-lès-Nancy, France, 2 Laboratory of Food Microbiology, Department of Food Science, Fundamental and Applied Research for Animal and Health, University of Liège, Liège, Belgium, 3 UMR1014 SECALIM, INRA, Oniris, Nantes, France, 4 Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg, Denmark, 5 Molecular Microbial Ecology Group, University of Copenhagen, Copenhagen, Edited by: Denmark Jennifer Ronholm, McGill University, Canada Reviewed by: Lactic acid bacteria (LAB) differ in their ability to colonize food and animal-associated Cristian Botta, habitats: while some species are specialized and colonize a limited number of habitats, University of Turin, Italy Rolf Dieter Joerger, other are generalist and are able to colonize multiple animal-linked habitats. In the University of Delaware, USA current study, Carnobacterium was used as a model genus to elucidate the genetic *Correspondence: basis of these colonization differences. Analyses of 16S rRNA gene meta-barcoding Frédéric Borges data showed that C. maltaromaticum followed by C. divergens are the most prevalent [email protected] species in foods derived from animals (meat, fish, dairy products), and in the gut. †Present address: Benoît Remenant, According to phylogenetic analyses, these two animal-adapted species belong to one Laboratoire de la Santé des Végétaux, of two deeply branched lineages. The second lineage contains species isolated from Agence Nationale de Sécurité Sanitaire de l’Alimentation, habitats where contact with animal is rare. Genome analyses revealed that members de l’Environnement et du Travail, of the animal-adapted lineage harbor a larger secretome than members of the other Angers, France lineage. The predicted cell-surface proteome is highly diversified in C. maltaromaticum Specialty section: and C. divergens with genes involved in adaptation to the animal milieu such as those This article was submitted to encoding biopolymer hydrolytic enzymes, a heme uptake system, and biopolymer- Food Microbiology, binding adhesins. These species also exhibit genes for gut adaptation and respiration. a section of the journal Frontiers in Microbiology In contrast, Carnobacterium species belonging to the second lineage encode a poorly Received: 29 November 2016 diversified cell-surface proteome, lack genes for gut adaptation and are unable to Accepted: 21 February 2017 respire. These results shed light on the important genomics traits required for adaptation Published: 08 March 2017 to animal-linked habitats in generalist Carnobacterium. Citation: Iskandar CF, Borges F, Taminiau B, Keywords: lactic acid bacteria, Carnobacterium, 16S meta-barcoding, comparative genomic analyses, ecological Daube G, Zagorec M, Remenant B, differentiation Leisner JJ, Hansen MA, Sørensen SJ, Mangavel C, Cailliez-Grimal C and INTRODUCTION Revol-Junelles A-M (2017) Comparative Genomic Analysis Lactic acid bacteria (LAB) include various genera and many species that have been investigated Reveals Ecological Differentiation in the Genus Carnobacterium. for decades because of their major role in food fermentations and their health benefit potential Front. Microbiol. 8:357. as probiotics. Understanding how LAB fitness can increase through evolution in these various doi: 10.3389/fmicb.2017.00357 habitats is critical for exploiting their beneficial properties. LAB are well-known for their ability Frontiers in Microbiology| www.frontiersin.org 1 March 2017| Volume 8| Article 357 fmicb-08-00357 March 6, 2017 Time: 15:38 # 2 Iskandar et al. Ecological Differentiation in Carnobacterium to colonize animal-derived food, i.e., meat, fish, and dairy as exemplified by Carnobacterium inhibens subsp. gilichinskyi products, and for being members of the gastrointestinal (GI) WN1359, Carnobacterium sp. 17-4, and Carnobacterium AT7 tract and the vagina microbiota (Douglas and Klaenhammer, which were isolated from Siberian permafrost, sea-ice from 2010; Douillard and de Vos, 2014). LAB can be divided into permanently cold fjords of the Arctic Ocean, and an oceanic specialized and generalist bacteria. Typically, the specialists that trench, respectively (Lauro et al., 2007; Voget et al., 2011; Leonard are used as starter cultures for a narrow range of fermented et al., 2013; Nicholson et al., 2015). Other species, including products are characterized by a low genetic diversity (Delorme C. maltaromaticum and C. divergens, have been found in animal- et al., 2010). Their genomes exhibit signs of massive losses associated habitats. These two species are the most frequently of genes involved in biosynthetic pathways (Douglas and isolated carnobacteria from various sources (Leisner et al., 2007) Klaenhammer, 2010). To compensate the loss of these functions, and belong to the dominant bacterial communities in meat genes encoding transporters for amino acids or carbohydrates and fish derived food (Chaillou et al., 2015; Duan et al., 2016; were gained to allow growth in nutritional rich fermentation Fougy et al., 2016; Jääskeläinen et al., 2016). These bacteria environments (Lorca et al., 2007). These genomic changes were are therefore very interesting models to investigate the genomic accompanied by a specialization to food matrices, particularly traits responsible for adaptation to animal-associated habitats. exemplified in dairy strains. Other LAB also exhibit genomes In the genus Carnobacterium, the genome size ranges from characteristic of their ecological specialization. Lactobacillus iners 2.4 Mbp for C. inhibens subsp. gilichinskyi WN1359 (Leonard is described to solely colonize the vaginal cavity and harbors et al., 2013), to 3.7 Mbp for C. maltaromaticum (Cailliez-Grimal one of the smallest LAB genomes presumably because its niche et al., 2013). It has been suggested that the larger genome of specialization allowed a substantial genome reduction (Macklaim the latter species is the basis of its success in colonizing various et al., 2011; Mendes-Soares et al., 2014). Another example is the habitats (Leisner et al., 2007). However, it appears that genome GI tract symbiont Lactobacillus reuteri, which is characterized size is not necessarily a predictor of the ability to occupy diverse by different lineages each one being apparently adapted to one habitats since the genome of C. divergens strains is relatively particular vertebrate host: rodent or human (Frese et al., 2011). small (∼2.7 Mbp), but this species is still able to colonize various By contrast, some species are more generalist in their ability habitats (Sun et al., 2015; Remenant et al., 2016). to colonize various environments and are therefore ubiquitous. The aim of this study was to investigate the ecological Species from the genus Enterococcus can be found in the niches Carnobacterium species can occupy and to identify GI tract of animals and in a multitude of fermented foods the genomic traits responsible for the high ecological success (Santagati et al., 2012). Their adaptation to various environments of some Carnobacterium species and the possible underlying is strongly linked to the presence in their genome of DNA adaptive mechanisms. For that purpose, we analyzed the acquired through horizontal gene transfer (HGT), resulting relative abundance of Carnobacterium species using 16S rDNA in a large pan genome (Santagati et al., 2012). Similarly, the metagenomic data. Subsequently, we compared the genomes genomes of some strains of the ubiquitous species Lactobacillus of Carnobacterium strains isolated from different environments rhamnosus encode multiple lifestyle traits allowing them to (mainly
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