[en] Lactic acid bacteria (LAB) differ in their ability to colonize food and animal-associated habitats: while some species are specialized and colonize a limited number of habitats, other are generalist and are able to colonize multiple animal-linked habitats. In the current study, Carnobacterium was used as a model genus to elucidate the genetic basis of these colonization differences. Analyses of 16S rRNA gene meta-barcoding data showed that C. maltaromaticum followed by C. divergens are the most prevalent species in foods derived from animals (meat, fish, dairy products), and in the gut. According to phylogenetic analyses, these two animal-adapted species belong to one of two deeply branched lineages. The second lineage contains species isolated from habitats where contact with animal is rare. Genome analyses revealed that members of the animal-adapted lineage harbor a larger secretome than members of the other lineage. The predicted cell-surface proteome is highly diversified in C. maltaromaticum and C. divergens with genes involved in adaptation to the animal milieu such as those encoding biopolymer hydrolytic enzymes, a heme uptake system, and biopolymer-binding adhesins. These species also exhibit genes for gut adaptation and respiration. In contrast, Carnobacterium species belonging to the second lineage encode a poorly diversified cell-surface proteome, lack genes for gut adaptation and are unable to respire. These results shed light on the important genomics traits required for adaptation to animal-linked habitats in generalist Carnobacterium.
Disciplines :
Microbiology
Author, co-author :
Iskandar, Christelle F.
Borges, Frederic
Taminiau, Bernard ; Université de Liège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Daube, Georges ; Université de Liège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Zagorec, Monique
Remenant, Benoit
Leisner, Jorgen J.
Hansen, Martin A.
Sorensen, Soren J.
Mangavel, Cecile
Cailliez-Grimal, Catherine
Revol-Junelles, Anne-Marie
Language :
English
Title :
Comparative Genomic Analysis Reveals Ecological Differentiation in the Genus Carnobacterium.
Alahuhta, M., Xu, Q., Brunecky, R., Adney, W. S., Ding, S.-Y., Himmel, M. E., et al. (2010). Structure of a fibronectin type III-like module from Clostridium thermocellum. Acta Cryst. F 66, 878-880. doi: 10.1107/S1744309110022529
Ammerman, J. W., and Azam, F. (1985). Bacterial 5-nucleotidase in aquatic ecosystems: a novel mechanism of phosphorus regeneration. Science 227, 1338-1340. doi: 10.1126/science.227.4692.1338
Balderas, M. A., Nobles, C. L., Honsa, E. S., Alicki, E. R., and Maresso, A. W. (2012). Hal is a Bacillus anthracis heme acquisition protein. J. Bacteriol. 194, 5513-5521. doi: 10.1128/JB.00685-12
Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., et al. (2007). CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709-1712. doi: 10.1126/science.1138140
Bengis-Garber, C., and Kushner, D. J. (1982). Role of membrane-bound 5'-nucleotidase in nucleotide uptake by the moderate halophile Vibrio costicola. J. Bacteriol. 149, 808-815
Bierne, H., and Cossart, P. (2007). Listeria monocytogenes surface proteins: from genome predictions to function. Microbiol. Mol. Biol. Rev. 71, 377-397. doi: 10.1128/MMBR.00039-06
Boekhorst, J., Helmer, Q., Kleerebezem, M., and Siezen, R. J. (2006a). Comparative analysis of proteins with a mucus-binding domain found exclusively in lactic acid bacteria. Microbiology 152, 273-280
Boekhorst, J., Wels, M., Kleerebezem, M., and Siezen, R. J. (2006b). The predicted secretome of Lactobacillus plantarum WCFS1 sheds light on interactions with its environment. Microbiology 152, 3175-3183
Brinster, S., Furlan, S., and Serror, P. (2007). C-terminal WxL domain mediates cell wall binding in Enterococcus faecalis and other gram-positive bacteria. J. Bacteriol. 189, 1244-1253. doi: 10.1128/JB.00773-06
Burgain, J., Scher, J., Lebeer, S., Vanderleyden, J., Cailliez-Grimal, C., Corgneau, M., et al. (2014). Significance of bacterial surface molecules interactions with milk proteins to enhance microencapsulation of Lactobacillus rhamnosus GG. Food Hydrocoll. 41, 60-70. doi: 10.1016/j.foodhyd.2014.03.029
Cailliez-Grimal, C., Afzal, M. I., and Revol-Junelles, A.-M. (2014). "Carnobacterium," in Encyclopedia of Food Microbiology, eds C. A. Batt and M. L. Tortorello (Cambridge, MA: Academic Press), 379-383. doi: 10.1016/B978-0-12-384730-0.00381-5
Cailliez-Grimal, C., Chaillou, S., Anba-Mondoloni, J., Loux, V., Afzal, M. I., Rahman, A., et al. (2013). Complete chromosome sequence of Carnobacterium maltaromaticum LMA 28. Genome Announc. 1:e00115-12. doi: 10.1128/genomeA.00115-12
Caspi, R., Altman, T., Billington, R., Dreher, K., Foerster, H., Fulcher, C. A., et al. (2014). The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 42, D459-D471. doi: 10.1093/nar/gkt1103
Chaillou, S., Chaulot-Talmon, A., Caekebeke, H., Cardinal, M., Christieans, S., Denis, C., et al. (2015). Origin and ecological selection of core and food-specific bacterial communities associated with meat and seafood spoilage. ISME J. 9, 1105-1118. doi: 10.1038/ismej.2014.202
Choby, J. E., and Skaar, E. P. (2016). Heme synthesis and acquisition in bacterial pathogens. J. Mol. Biol. 428, 3408-3428. doi: 10.1016/j.jmb.2016.03.018
Christensen, J. E., Dudley, E. G., Pederson, J. A., and Steele, J. L. (1999). Peptidases and amino acid catabolism in lactic acid bacteria. Antonie Van Leeuwenhoek 76, 217-246. doi: 10.1023/A:1002001919720
Comfort, D., and Clubb, R. T. (2004). A comparative genome analysis identifies distinct sorting pathways in Gram-positive bacteria. Infect. Immun. 72, 2710-2722. doi: 10.1128/IAI.72.5.2710-2722.2004
Delorme, C., Bartholini, C., Bolotine, A., Ehrlich, S. D., and Renault, P. (2010). Emergence of a cell wall protease in the Streptococcus thermophilus population. Appl. Environ. Microbiol. 76, 451-460. doi: 10.1128/AEM.01018-09
Doeven, M. K., Kok, J., and Poolman, B. (2005). Specificity and selectivity determinants of peptide transport in Lactococcus lactis and other microorganisms: peptide transport in Lactococcus lactis. Mol. Microbiol. 57, 640-649. doi: 10.1111/j.1365-2958.2005.04698.x
Douglas, G. L., and Klaenhammer, T. R. (2010). Genomic evolution of domesticated microorganisms. Annu. Rev. Food Sci. Technol. 1, 397-414. doi: 10.1146/annurev.food.102308.124134
Douillard, F. P., and de Vos, W. M. (2014). Functional genomics of lactic acid bacteria: from food to health. Microb. Cell Fact. 13:S8. doi: 10.1186/1475-2859-13-S1-S8
Douillard, F. P., Ribbera, A., Kant, R., Pietila, T. E., Jarvinen, H. M., Messing, M., et al. (2013). Comparative genomic and functional analysis of 100 Lactobacillus rhamnosus strains and their comparison with strain GG. PLoS Genet. 9:e1003683. doi: 10.1371/journal.pgen.1003683
Duan, S., Hu, X., Li, M., Miao, J., Du, J., and Wu, R. (2016). Composition and metabolic activities of the bacterial community in shrimp sauce at the flavor-forming stage of fermentation as revealed by metatranscriptome and 16S rRNA gene sequencing. J. Agric. Food Chem. 64, 2591-2603. doi: 10.1021/acs.jafc.5b05826
Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200. doi: 10.1093/bioinformatics/btr381
Elasri, M. O., Thomas, J. R., Skinner, R. A., Blevins, J. S., Beenken, K. E., Nelson, C. L., et al. (2002). Staphylococcus aureus collagen adhesin contributes to the pathogenesis of osteomyelitis. Bone 30, 275-280. doi: 10.1016/S8756-3282(01)00632-9
Fougy, L., Desmonts, M.-H., Coeuret, G., Fassel, C., Hamon, E., Hézard, B., et al. (2016). Reducing salt in raw pork sausages increases spoilage and correlates with reduced bacterial diversity. Appl. Environ. Microbiol. 82, 3928-3939. doi: 10.1128/AEM.00323-16
Frese, S. A., Benson, A. K., Tannock, G. W., Loach, D. M., Kim, J., Zhang, M., et al. (2011). The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. PLOS Genet. 7:e1001314. doi: 10.1371/journal.pgen.1001314
Galloway-Peña, J. R., Liang, X., Singh, K. V., Yadav, P., Chang, C., Rosa, S. L. L., et al. (2015). The identification and functional characterization of WxL proteins from Enterococcus faecium reveal surface proteins involved in extracellular matrix interactions. J. Bacteriol. 197, 882-892. doi: 10.1128/JB.02288-14
Gaudin, C. F. M., Grigg, J. C., Arrieta, A. L., and Murphy, M. E. P. (2011). Unique heme-iron coordination by the hemoglobin receptor IsdB of Staphylococcus aureus. Biochemistry 50, 5443-5452. doi: 10.1021/bi200369p
Hiu, S. F., Holt, R. A., Sriranganathan, N., Seidler, R. J., and Fryer, J. L. (1984). Lactobacillus piscicola, a new species from salmonid fish. Int. J. Syst. Bacteriol. 34, 393-400. doi: 10.1099/00207713-34-4-393
Iskandar, C. F., Cailliez-Grimal, C., Rahman, A., Rondags, E., Remenant, B., Zagorec, M., et al. (2016). Genes associated to lactose metabolism illustrate the high diversity of Carnobacterium maltaromaticum. Food Microbiol. 58, 79-86. doi: 10.1016/j.fm.2016.03.008
Jääskeläinen, E., Hultman, J., Parshintsev, J., Riekkola, M.-L., and Björkroth, J. (2016). Development of spoilage bacterial community and volatile compounds in chilled beef under vacuum or high oxygen atmospheres. Int. J. Food Microbiol. 223, 25-32. doi: 10.1016/j.ijfoodmicro.2016.01.022
Kanehisa, M., and Goto, S. (2000). KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30. doi: 10.1093/nar/28.1.27
Kanehisa, M., Goto, S., Sato, Y., Kawashima, M., Furumichi, M., and Tanabe, M. (2014). Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 42, D199-D205. doi: 10.1093/nar/gkt1076
Kleerebezem, M., Hols, P., Bernard, E., Rolain, T., Zhou, M., Siezen, R. J., et al. (2010). The extracellular biology of the Lactobacilli. FEMS Microbiol. Rev. 34, 199-230. doi: 10.1111/j.1574-6976.2009.00208.x
Kunji, E. R., Mierau, I., Hagting, A., Poolman, B., and Konings, W. N. (1996). The proteolytic systems of lactic acid bacteria. Antonie Van Leeuwenhoek 70, 187-221. doi: 10.1007/BF00395933
Lauro, F. M., Chastain, R. A., Blankenship, L. E., Yayanos, A. A., and Bartlett, D. H. (2007). The unique 16S rRNA genes of piezophiles reflect both phylogeny and adaptation. Appl. Environ. Microbiol. 73, 838-845. doi: 10.1128/AEM.01726-06
Laursen, B. G., Bay, L., Cleenwerck, I., Vancanneyt, M., Swings, J., Dalgaard, P., et al. (2005). Carnobacterium divergens and Carnobacterium maltaromaticum as spoilers or protective cultures in meat and seafood: phenotypic and genotypic characterization. Syst. Appl. Microbiol. 28, 151-164. doi: 10.1016/j.syapm.2004.12.001
Lechardeur, D., Cesselin, B., Fernandez, A., Lamberet, G., Garrigues, C., Pedersen, M., et al. (2011). Using heme as an energy boost for lactic acid bacteria. Curr. Opin. Biotechnol. 22, 143-149. doi: 10.1016/j.copbio.2010.12.001
Leisner, J. J., Hansen, M. A., Larsen, M. H., Hansen, L., Ingmer, H., and Sørensen, S. J. (2012). The genome sequence of the lactic acid bacterium, Carnobacterium maltaromaticum ATCC 35586 encodes potential virulence factors. Int. J. Food Microbiol. 152, 107-115. doi: 10.1016/j.ijfoodmicro.2011.05.012
Leisner, J. J., Laursen, B. G., Prévost, H., Drider, D., and Dalgaard, P. (2007). Carnobacterium: positive and negative effects in the environment and in foods. FEMS Microbiol. Rev. 31, 592-613. doi: 10.1111/j.1574-6976.2007.00080.x
Leonard, M. T., Panayotova, N., Farmerie, W. G., Triplett, E. W., and Nicholson, W. L. (2013). Complete genome sequence of Carnobacterium gilichinskyi strain WN1359T (DSM 27470T). Genome Announc. 1:e00985-13. doi: 10.1128/genomeA.00985-13
Lorca, G. L., Barabote, R. D., Zlotopolski, V., Tran, C., Winnen, B., Hvorup, R. N., et al. (2007). Transport capabilities of eleven gram-positive bacteria: comparative genomic analyses. Biochim. Biophys. Acta 1768, 1342-1366. doi: 10.1016/j.bbamem.2007.02.007
Lukic, J., Strahinic, I., Jovcic, B., Filipic, B., Topisirovic, L., Kojic, M., et al. (2012). Different roles for lactococcal aggregation factor and mucin binding protein in adhesion to gastrointestinal mucosa. Appl. Environ. Microbiol. 78, 7993-8000. doi: 10.1128/AEM.02141-12
Macklaim, J. M., Gloor, G. B., Anukam, K. C., Cribby, S., and Reid, G. (2011). At the crossroads of vaginal health and disease, the genome sequence of Lactobacillus iners AB-1. Proc. Natl. Acad. Sci. U.S.A. 108, 4688-4695. doi: 10.1073/pnas.1000086107
Mandlik, A., Das, A., and Ton-That, H. (2008). The molecular switch that activates the cell wall anchoring step of pilus assembly in gram-positive bacteria. Proc. Natl. Acad. Sci. U.S.A. 105, 14147-14152. doi: 10.1073/pnas.0806350105
Maresso, A. W., and Schneewind, O. (2008). Sortase as a target of anti-infective therapy. Pharmacol. Rev. 60, 128-141. doi: 10.1124/pr.107.07110
Martino, M. E., Bayjanov, J. R., Caffrey, B. E., Wels, M., Joncour, P., Hughes, S., et al. (2016). Nomadic lifestyle of Lactobacillus plantarum revealed by comparative genomics of 54 strains isolated from different habitats. Environ. Microbiol. 18, 4974-4989. doi: 10.1111/1462-2920.13455
Meisel, J., Wolf, G., and Hammes, W. P. (1994). Heme-dependent cytochrome formation in Lactobacillus maltaromicus. Syst. Appl. Microbiol. 17, 20-23. doi: 10.1016/S0723-2020(11)80026-3
Mendes-Soares, H., Suzuki, H., Hickey, R. J., and Forney, L. J. (2014). Comparative functional genomics of Lactobacillus spp. reveals possible mechanisms for specialization of vaginal Lactobacilli to their environment. J. Bacteriol. 196, 1458-1470. doi: 10.1128/JB.01439-13
Miller, A., Morgan, M. E., and Libbey, L. M. (1974). Lactobacillus maltaromicus, a new species producing a malty aroma. Int. J. Syst. Bacteriol. 24, 346-354. doi: 10.1099/00207713-24-3-346
Millière, J. B., Michel, M., Mathieu, F., and Lefebvre, G. (1994). Presence of Carnobacterium spp. in French surface mould-ripened soft-cheese. J. Appl. Bacteriol. 76, 264-269. doi: 10.1111/j.1365-2672.1994.tb01626.x
Nicholson, W. L., Zhalnina, K., de Oliveira, R. R., and Triplett, E. W. (2015). Proposal to rename Carnobacterium inhibens as Carnobacterium inhibens subsp inhibens subsp nov and description of Carnobacterium inhibens subsp gilichinskyi subsp nov., a psychrotolerant bacterium isolated from Siberian permafrost. Int. J. Syst. Evol. Microbiol. 65, 556-561. doi: 10.1099/ijs.0.067983-0
Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011). SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Meth. 8, 785-786. doi: 10.1038/nmeth.1701
Pikuta, E. V. (2014). The Family Carnobacteriaceae, eds W. H. Holzapfel and B. J. B. Wood (Oxford: Blackwell Science Publishers). doi: 10.1002/9781118655252.part2
Pikuta, E. V., and Hoover, R. B. (2014). The Genus Carnobacterium, eds W. H. Holzapfel and B. J. B. Wood (Oxford: Blackwell Science Publishers). doi: 10.1002/9781118655252.ch10
Pilet, M. F., Dousset, X., Barré, R., Novel, G., Desmazeaud, M., and Piard, J. C. (1994). Evidence for two bacteriocins produced by Carnobacterium piscicola and Carnobacterium divergens isolated from fish and active against Listeria monocytogenes. J. Food Prot. 58, 256-262. doi: 10.4315/0362-028X-58.3.256
Proft, T., and Baker, E. N. (2009). Pili in Gram-negative and Gram-positive bacteria-structure, assembly and their role in disease. Cell. Mol. Life Sci. 66, 613-635. doi: 10.1007/s00018-008-8477-4
Rahman, A., Cailliez-Grimal, C., Bontemps, C., Payot, S., Chaillou, S., Revol-Junelles, A.-M., et al. (2014a). High genetic viversity among strains of the unindustrialized lactic acid bacterium Carnobacterium maltaromaticum in dairy products as revealed by multilocus sequence typing. Appl. Environ. Microbiol. 80, 3920-3929. doi: 10.1128/AEM.00681-14
Rahman, A., Gleinser, M., Lanhers, M.-C., Riedel, C. U., Foligne, B., Hanse, M., et al. (2014b). Adaptation of the lactic acid bacterium Carnobacterium maltaromaticum LMA 28 to the mammalian gastrointestinal tract: from survival in mice to interaction with human cells. Int. Dairy J. 34, 93-99. doi: 10.1016/j.idairyj.2013.07.003
Remenant, B., Borges, F., Cailliez-Grimal, C., Revol-Junelles, A.-M., Marché, L., Lajus, A., et al. (2016). Draft genome sequence of Carnobacterium divergens V41, a bacteriocin-producing strain. Genome Announc. 4:e01109-16. doi: 10.1128/genomeA.01109-16
Rezaïki, L., Lamberet, G., Derré, A., Gruss, A., and Gaudu, P. (2008). Lactococcus lactis produces short-chain quinones that cross-feed Group B Streptococcus to activate respiration growth. Mol. Microbiol. 67, 947-957. doi: 10.1111/j.1365-2958.2007.06083.x
Rodriguez, C., Taminiau, B., Brévers, B., Avesani, V., Van Broeck, J., Leroux, A., et al. (2015). Faecal microbiota characterisation of horses using 16 rdna barcoded pyrosequencing, and carriage rate of Clostridium difficile at hospital admission. BMC Microbiol. 15:181. doi: 10.1186/s12866-015-0514-5
Santagati, M., Campanile, F., and Stefani, S. (2012). Genomic diversification of enterococci in hosts: the role of the mobilome. Front. Microbiol. 3:95. doi: 10.3389/fmicb.2012.00095
Savijoki, K., Ingmer, H., and Varmanen, P. (2006). Proteolytic systems of lactic acid bacteria. Appl. Microbiol. Biotechnol. 71, 394-406. doi: 10.1007/s00253-006-0427-1
Schloss, P. D., and Handelsman, J. (2003). Biotechnological prospects from metagenomics. Curr. Opin. Biotechnol. 14, 303-310. doi: 10.1016/S0958-1669(03)00067-3
Schneewind, O., and Missiakas, D. (2014). Sec-secretion and sortase-mediated anchoring of proteins in Gram-positive bacteria. Biochim. Biophys. Acta 1843, 1687-1697. doi: 10.1016/j.bbamcr.2013.11.009
Seedorf, H., Griffin, N. W., Ridaura, V. K., Reyes, A., Cheng, J., Rey, F. E., et al. (2014). Bacteria from diverse habitats colonize and compete in the mouse gut. Cell 159, 253-266. doi: 10.1016/j.cell.2014.09.008
Siezen, R., Boekhorst, J., Muscariello, L., Molenaar, D., Renckens, B., and Kleerebezem, M. (2006). Lactobacillus plantarum gene clusters encoding putative cell-surface protein complexes for carbohydrate utilization are conserved in specific gram-positive bacteria. BMC Genomics 7:126. doi: 10.1186/1471-2164-7-126
Siezen, R. J. (1999). Multi-domain, cell-envelope proteinases of lactic acid bacteria. Antonie Van Leeuwenhoek 76, 139-155. doi: 10.1023/A:1002036906922
Sun, C., Fukui, H., Hara, K., Kitayama, Y., Eda, H., Yang, M., et al. (2015). Expression of Reg family genes in the gastrointestinal tract of mice treated with indomethacin. Am. J. Physiol. Gastrointest. Liver Physiol. 308, G736-G744. doi: 10.1152/ajpgi.00362.2014
Tailford, L. E., Crost, E. H., Kavanaugh, D., and Juge, N. (2015). Mucin glycan foraging in the human gut microbiome. Front. Genet. 6:81. doi: 10.3389/fgene.2015.00081
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
Vallenet, D., Belda, E., Calteau, A., Cruveiller, S., Engelen, S., Lajus, A., et al. (2013). MicroScope-an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Nucleic Acids Res. 41, D636-D647. doi: 10.1093/nar/gks1194
Voget, S., Klippel, B., Daniel, R., and Antranikian, G. (2011). Complete genome sequence of Carnobacterium sp 17-4. J. Bacteriol. 193, 3403-3404. doi: 10.1128/JB.05113-11
Zhou, Y., Liang, Y., Lynch, K. H., Dennis, J. J., and Wishart, D. S. (2011). PHAST: a fast phage search tool. Nucleic Acids Res. 39, W347-W352. doi: 10.1093/nar/gkr485
