[en] Microbiome studies generally focus on the gut microbiome, which is composed of a large proportion of commensal bacteria. Here we propose a first analysis of the liver microbiomeusing next generation sequencing as a tool to detect potentially pathogenic strains. We used Peromyscus leucopus, the main reservoir host species of Lyme disease in eastern North America, as a model and sequenced V5-V6 regions of the 16S gene from 18 populations in southern Quebec (Canada). The Lactobacillus genus was found to dominate the liver microbiome.We also detected a large proportion of individuals infected by Bartonella vinsonii arupensis, a human pathogenic bacteria responsible for endocarditis, aswell as Borrelia burgdorferi, the pathogen responsible for Lyme disease in North America. We then compared the microbiomes among two P. leucopus genetic clusters occurring on either side of the St. Lawrence River, and did not detect any effect of the host genotype on their liver microbiome assemblage. Finally, we report, for the first time, the presence of B. burgdorferi in a smallmammal host fromthe northern side of the St. Lawrence River, in support of models that have predicted the northern spread of Lyme disease in Canada.
Disciplines :
Microbiology
Author, co-author :
André, Adrien ; Université de Liège > Département des sciences de la vie > Génétique et physiologie des microalgues
Mouton, Alice ; Université de Liège > Département des sciences de la vie > Génétique et physiologie des microalgues
millien, virginie
Michaux, Johan ; Université de Liège > Département des sciences de la vie > Génétique et physiologie des microalgues
Language :
English
Title :
Liver microbiome of Peromyscus leucopus, a key reservoir host species for emerging infectious diseases in North America
Alternative titles :
[fr] le microbiome du foie de Peromyscus leucopus, une espèce réservoir clé pour les maladies infectieuses en Amérique du Nord.
Publication date :
13 April 2017
Journal title :
Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics of Infectious Diseases
ISSN :
1567-1348
eISSN :
1567-7257
Publisher :
Elsevier
Peer reviewed :
Peer Reviewed verified by ORBi
Tags :
CÉCI : Consortium des Équipements de Calcul Intensif
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE] CÉCI - Consortium des Équipements de Calcul Intensif [BE] NSERC - Natural Sciences and Engineering Research Council [CA]
Andersson, A.F., Lindberg, M., Jakobsson, H., Bäckhed, F., Nyrén, P., Engstrand, L., Comparative analysis of human gut microbiota by barcoded pyrosequencing. PloS one, 3(7), 2008 e2836.
Aroutcheva, A., Gariti, D., Simon, M., Shott, S., Faro, J., Simoes, J.A., Gurguis, A., Faro, S., Defense factors of vaginal lactobacilli. Am. J. Obstet. Gynecol. 185 (2001), 375–379.
Bai, Y., Calisher, C.H., Kosoy, M.Y., Root, J.J., Doty, J.B., Persistent infection or successive reinfection of deer mice with Bartonella vinsonii subsp. arupensis. Appl. Environ. Microbiol. 77 (2011), 1728–1731.
Balzan, S., De Almeida Quadros, C., De Cleva, R., Zilberstein, B., Cecconello, I., Bacterial translocation: overview of mechanisms and clinical impact. J. Gastroenterol. Hepatol. 22 (2007), 464–471.
Baxter, N.T., Wan, J.J., Schubert, A.M., Jenior, M.L., Myers, P., Schloss, P.D., Intra- and interindividual variations mask interspecies variation in the microbiota of sympatric peromyscus populations. Appl. Environ. Microbiol. 81 (2015), 396–404.
Breitschwerdt, E.B., Kordick, D.L., Bartonella infection in animals: carriership, reservoir potential, pathogenicity, and zoonotic potential for human infection. Clin. Microbiol. Rev. 13 (2000), 428–438.
Can, I., Javan, G.T., Pozhitkov, A.E., Noble, P.A., Distinctive thanatomicrobiome signatures found in the blood and internal organs of humans. J. Microbiol. Methods 106 (2014), 1–7.
Casswall, T.H., Nemeth, A., Nilsson, I., Wadstrom, T., Nilsson, H.O., Helicobacter species DNA in liver and gastric tissues in children and adolescents with chronic liver disease. Scand. J. Gastroenterol. 45 (2010), 160–167.
Dickson, R.P., Huffnagle, G.B., The lung microbiome: new principles for respiratory bacteriology in health and disease. PLoS Pathog., 11, 2015, e1004923.
Dykhuizen, D.E., Brisson, D., Sandigursky, S., Wormser, G.P., Nowakowski, J., Nadelman, R.B., Schwartz, I., The propensity of different Borrelia burgdorferi sensu stricto genotypes to cause disseminated infections in humans. Am. J. Trop. Med. Hyg. 78:5 (2008), 806–810.
Ebady, R., Niddam, A.F., Boczula, A.E., Kim, Y.R., Gupta, N., Tang, T.T., Moriarty, T.J., Biomechanics of Borrelia burgdorferi vascular interactions. Cell Reports 16:10 (2016), 2593–2604.
Edgar, R.C., Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26 (2010), 2460–2461.
Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., Knight, R., UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27 (2011), 2194–2200.
Edouard, S., Nabet, C., Lepidi, H., Fournier, P.E., Raoult, D., Bartonella, a common cause of endocarditis: a report on 106 cases and review. J. Clin. Microbiol. 53 (2015), 824–829.
Fenollar, F., Sire, S., Raoult, D., Bartonella vinsonii subsp. arupensis as an agent of blood culture-negative endocarditis in a human. J. Clin. Microbiol. 43 (2005), 945–947.
Fiset, J., Tessier, N., Millien, V., Lapointe, F.J., Phylogeographic structure of the white-footed mouse and the deer mouse, two Lyme disease reservoir hosts in Quebec. PLoS One, 10, 2015, e0144112.
Galan, M., Razzauti, M., Bard, E., Bernard, M., Brouat, C., Charbonnel, N., Dehne-Garcia, A., Loiseau, A., Tatard, C., Tamisier, L., Vayssier-Taussat, M., Vignes, H., Cosson, J.-F., Bik, H., 16S rRNA Amplicon Sequencing for Epidemiological Surveys of Bacteria in Wildlife. mSystems 1. 2016 (e00032-00016).
Gaulin, C., Leblanc, M.A., Mercier, M., Valiquette, L., Bédard, D., Markowski, F., Lambert, L., Petit, G., Poirier, B., Picard, I., Flash vigie. Bulletin québécois de vigie, de surveillance et d'intervention en protection de la santé publique, 11, 2016.
Gibson, R.L., Burns, J.L., Ramsey, B.W., Pathophysiology and management of pulmonary infections in cystic fibrosis. Am. J. Respir. Crit. Care Med. 168 (2003), 918–951.
Goodrich, Julia K., Waters, Jillian L., Poole, Angela C., Sutter, Jessica L., Koren, O., Blekhman, R., Beaumont, M., Van Treuren, W., Knight, R., Bell, Jordana T., Spector, Timothy D., Clark, Andrew G., Ley, Ruth E., Human genetics shape the gut microbiome. Cell 159 (2014), 789–799.
Gulia-Nuss, M., Nuss, A.B., Meyer, J.M., Sonenshine, D.E., Roe, R.M., Waterhouse, R.M., Sattelle, D.B., de la Fuente, J., Ribeiro, J.M., Megy, K., Thimmapuram, J., Miller, J.R., Walenz, B.P., Koren, S., Hostetler, J.B., Thiagarajan, M., Joardar, V.S., Hannick, L.I., Bidwell, S., Hammond, M.P., Young, S., Zeng, Q., Abrudan, J.L., Almeida, F.C., Ayllón, N., Bhide, K., Bissinger, B.W., Bonzon-Kulichenko, E., Buckingham, S.D., Caffrey, D.R., Caimano, M.J., Croset, V., Driscoll, T., Gilbert, D., Gillespie, J.J., Giraldo-Calderón, G.I., Grabowski, J.M., Jiang, D., Khalil, S.M.S., Kim, D., Kocan, K.M., Koči, J., Kuhn, R.J., Kurtti, T.J., Lees, K., Lang, E.G., Kennedy, R.C., Kwon, H., Perera, R., Qi, Y., Radolf, J.D., Sakamoto, J.M., Sánchez-Gracia, A., Severo, M.S., Silverman, N., Šimo, L., Tojo, M., Tornador, C., Van Zee, J.P., Vázquez, J., Vieira, F.G., Villar, M., Wespiser, A.R., Yang, Y., Zhu, J., Arensburger, P., Pietrantonio, P.V., Barker, S.C., Shao, R., Zdobnov, E.M., Hauser, F., Grimmelikhuijzen, C.J.P., Park, Y., Rozas, J., Benton, R., Pedra, J.H.F., Nelson, D.R., Unger, M.F., Tubio, J.M.C., Tu, Z., Robertson, H.M., Shumway, M., Sutton, G., Wortman, J.R., Lawson, D., Wikel, S.K., Nene, V.M., Fraser, C.M., Collins, F.H., Birren, B., Nelson, K.E., Caler, E., Hill, C.A., Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nat. Commun., 7, 2016, 10507.
Haas, B.J., Gevers, D., Earl, A.M., Feldgarden, M., Ward, D.V., Giannoukos, G., Ciulla, D., Tabbaa, D., Highlander, S.K., Sodergren, E., Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21 (2011), 494–504.
Hofmeister, E.K., Kolbert, C.P., Abdulkarim, A.S., Magera, J.M., Hopkins, M.K., Uhl, J.R., Ambyaye, A., Telford, S.R. 3rd, Cockerill, F.R. 3rd, Persing, D.H., Cosegregation of a novel Bartonella species with Borrelia burgdorferi and Babesia microti in Peromyscus leucopus. J. Infect. Dis. 177 (1998), 409–416.
Johnson, P.T.J., De Roode, J.C., Fenton, A., Why infectious disease research needs community ecology. Science, 349, 2015.
Karesh, W.B.D., Andy, Lloyd-Smith, James O., Lubroth, Juan, Dixon, Matthew A., Bennett, Malcolm, Aldrich, Stephen, Harrington Pierre, T.F., Loh, Elizabeth H., Machalaba, Catherine C., Thomas, Mathew Jason, Heymann, David L., Ecology of zoonoses: natural and unnatural histories. Publ. Health Resour. Pap., 296, 2012.
Ledevin, R., Millien, V., Congruent morphological and genetic differentiation as a signature of range expansion in a fragmented landscape. Ecol. Evol. 3 (2013), 4172–4182.
Leo, S.T., Gonzalez, A., Millien, V., Genetic signature of range expansion in a disease vector. J. Hered., 2016, 10.1093/jherd/esw073.
Ley, R.E., Bäckhed, F., Turnbaugh, P., Lozupone, C.A., Knight, R.D., Gordon, J.I., Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 11070–11075.
Linnenbrink, M., Wang, J., Hardouin, E.A., Kunzel, S., Metzler, D., Baines, J.F., The role of biogeography in shaping diversity of the intestinal microbiota in house mice. Mol. Ecol. 22 (2013), 1904–1916.
Lozano, R., Naghavi, M., Foreman, K., et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the global burden of disease study 2010. Lancet, 380, 2013, 2095.
Lozupone, C., Knight, R., UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71 (2005), 8228–8235.
Lynch, M.F., Tauxe, R.V., Hedberg, C.W., The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiol. Infect. 137 (2009), 307–315.
Maggi, R.G., Breitschwerdt, E.B., Potential limitations of the 16S-23S rRNA intergenic region for molecular detection of Bartonella species. J. Clin. Microbiol. 43 (2005), 1171–1176.
Mather, T.N., Wilson, M.L., Moore, S.I., Ribeiro, J.M.C., Spielman, A., Comparing the relative potential of rodents as reservoirs of the Lyme disease spirochete (Borrelia burgdorferi). Am. J. Epidemiol. 130 (1989), 143–150.
McMurdie, P.J., Holmes, S., phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE, 8(4), 2013.
Melzi, M.L., Ferrari, G.M., D'Adda, A., Bovo, G., Foresti, S., Cavallero, A., Biondi, A., Hepatic granulomatous lesions caused by systemic Bartonella vinsonii subsp. arupensis infection in a child. Pediatr. Infect. Dis. J. 34:12 (2015), 1416–1417.
Minard, G., Tran, F.H., Van, V.T., Goubert, C., Bellet, C., Lambert, G., Kim, K.L., Thuy, T.H., Mavingui, P., Valiente Moro, C., French invasive Asian tiger mosquito populations harbor reduced bacterial microbiota and genetic diversity compared to Vietnamese autochthonous relatives. Front. Microbiol., 6, 2015, 970.
Moeller, A.H., Peeters, M., Ndjango, J.B., Li, Y., Hahn, B.H., Ochman, H., Sympatric chimpanzees and gorillas harbor convergent gut microbial communities. Genome Res. 23 (2013), 1715–1720.
Ochman, H., Worobey, M., Kuo, C.-H., Ndjango, J.-B., Peeters, M., Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol., 8(11), 2010.
Ogden, N.H., Margos, G., Aanensen, D.M., Drebot, M.A., Feil, E.J., Hanincova, K., Lindsay, L.R., Investigation of genotypes of Borrelia burgdorferi in Ixodes scapularis ticks collected during surveillance in Canada. Appl. Environ. Microbiol. 77:10 (2011), 3244–3254.
Ostfeld, R.S., Lyme Disease: The Ecology of a Complex System. 2011, Oxford University Press, 216.
Ostfeld, R.S., Levi, T., Jolles, A.E., Martin, L.B., Hosseini, P.R., Keesing, F., Life history and demographic drivers of reservoir competence for three tick-borne zoonotic pathogens. PLoS One, 9, 2014, e107387.
Phillips, C.D., Phelan, G., Dowd, S.E., McDonough, M.M., Ferguson, A.W., Delton Hanson, J., Siles, L., Ordonez-Garza, N., San Francisco, M., Baker, R.J., Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography. Mol. Ecol. 21 (2012), 2617–2627.
Radolf, J.D., Caimano, M.J., Stevenson, B., Hu, L.T., Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease Spirochaetes. Nat. Rev. Microbiol. 10 (2012), 87–99.
Rajaram, S., Oono, Y., NeatMap-non-clustering heat map alternatives in R. BMC bioinformatics, 11(1), 2010, 45.
Rogic, A., Tessier, N., Legendre, P., Lapointe, F.J., Millien, V., Genetic structure of the white-footed mouse in the context of the emergence of Lyme disease in southern Quebec. Ecol. Evol. 3 (2013), 2075–2088.
Roy-Dufresne, E., Logan, T., Simon, J.A., Chmura, G.L., Millien, V., Poleward expansion of the white-footed mouse Peromyscus leucopus under climate change: implications for the spread of Lyme disease. PLoS One, 8, 2013, e80724.
Sanders, J.G., Beichman, A.C., Roman, J., Scott, J.J., Emerson, D., McCarthy, J.J., Girguis, P.R., Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores. Nat. Commun., 6, 2015, 8285.
Simon, J.A., Marrotte, R.R., Desrosiers, N., Fiset, J., Gaitan, J., Gonzalez, A., Koffi, J.K., Lapointe, F.-J., Leighton, P.A., Lindsay, L.R., Logan, T., Milord, F., Ogden, N.H., Rogic, A., Roy-Dufresne, E., Suter, D., Tessier, N., Millien, V., Climate change and habitat fragmentation drive the occurrence of Borrelia burgdorferi, the agent of Lyme disease, at the northeastern limit of its distribution. Evol. Appl. 7 (2014), 750–764.
R Core Team, R: A Language and Environment for Statistical Computing. 2016, R Foundation for Statistical Computing, Vienna, Austria URL: https://www.R-project.org.
Turnbaugh, P.J., Ridaura, V.K., Faith, J.J., Rey, F.E., Knight, R., Gordon, J.I., The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med., 2009, 1.
Walter, J., Ecological role of Lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl. Environ. Microbiol. 74 (2008), 4985–4996.
Wang, Q., Garrity, G.M., Tiedje, J.M., Cole, J.R., Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73 (2007), 5261–5267.
Weinstock, G.M., Genomic approaches to studying the human microbiota. Nature 489 (2012), 250–256.
Welch, D.F., C., K., Hofmeister, E.K., Persing, D.H., Robison, D.A., Steigerwalt, A.G., Isolation of a new subspecies, Bartonella vinsonii subsp. arupensis, from a cattle rancher: identity with isolates found in conjunction with Borrelia burgdorferi and Babesia microti among naturally infected mice. J. Clin. Microbiol. 37 (1999), 2598–2601.
Yun, Y., Srinivas, G., Kuenzel, S., Linnenbrink, M., Alnahas, S., Bruce, K.D., Steinhoff, U., Baines, J.F., Schaible, U.E., Environmentally determined differences in the murine lung microbiota and their relation to alveolar architecture. PLoS One, 9, 2014, e113466.
