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Distinct gut microbiotas between southern elephant seals and Weddell seals of Antarctica

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Abstract

The gut microbiome provides ecological information about host animals, but we still have limited knowledge of the gut microbiome, particularly for animals inhabiting remote locations, such as Antarctica. Here, we compared fecal microbiota between southern elephant seals (Mirounga leonina) and Weddell seals (Leptonychotes weddelli), that are top predatory marine mammals in the Antarctic ecosystem, using 16S rRNA amplicon sequencing and assessed the relationships of the gut microbial communities to functional profiles using gut metabolite analysis. The bacterial community did not differ significantly by host species or sex at the phylum level, but the distinction at the family level was obvious. The family Ruminococcaceae (Firmicutes) was more abundant in southern elephant seals than in Weddell seals, and the families Acidaminococcaceae (Firmicutes) and Pasteurellaceae (Gammaproteobacteria) were uniquely present in Weddell seals. The fecal bacterial community structure was distinctively clustered by host species, with only 6.7% of amplicon sequence variants (ASVs) shared between host species. This result implies that host phylogeny rather than other factors, such as diet or age, could be the major driver of fecal microbiotic diversification. Interestingly, there was no apparent sex effect on bacterial community structure in Weddell seals, but the effect of sex was pronounced in adult southern elephant seals mainly due to the prevalence of Edwardsiella sp., suggesting that extreme sexual dimorphism may modulate the gut microbiota of southern elephant seals. Unlike the clear distinction in the taxonomic composition of fecal bacterial communities, there were no discernible differences in the profiles of potential microbial functions and gut metabolites between host species or sexes, indicating that functional redundancy dominates the gut microbiota of seals surveyed in this study.

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References

  • Anderson, M.J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46.

    Google Scholar 

  • Arnason, U., Gullberg, A., Janke, A., Kullberg, M., Lehman, N., Petrov, E.A., and Väinölä, R. 2006. Pinniped phylogeny and a new hypothesis for their origin and dispersal. Mol. Phylogenet. Evol. 41, 345–354.

    Article  PubMed  Google Scholar 

  • Bäckhed, F., Fraser, C.M., Ringel, Y., Sanders, M.E., Sartor, R.B., Sherman, P.M., Versalovic, J., Young, V., and Finlay, B.B. 2012. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe 12, 611–622.

    Article  CAS  PubMed  Google Scholar 

  • Banks, J.C., Cary, S.C., and Hogg, I.D. 2014. Isolated faecal bacterial communities found for Weddell seals, Leptonychotes weddellii, at White Island, McMurdo Sound, Antarctica. Polar Biol. 37, 1857–1864.

    Article  Google Scholar 

  • Barko, P.C., McMichael, M.A., Swanson, K.S., and Williams, D.A. 2018. The gastrointestinal microbiome: a review. J. Vet. Intern. Med. 32, 9–25.

    Article  CAS  PubMed  Google Scholar 

  • Bik, E.M., Costello, E.K., Switzer, A.D., Callahan, B.J., Holmes, S.P., Wells, R.S., Carlin, K.P., Jensen, E.D., Venn-Watson, S., and Relman, D.A. 2016. Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea. Nat. Commun. 7, 10516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowen, W.D. 1997. Role of marine mammals in aquatic ecosystems. Mar. Ecol. Prog. 158, 267–274.

    Article  Google Scholar 

  • Bradshaw, C.J.A., Hindell, M.A., Best, N.J., Phillips, K.L., Wilson, G., and Nichols, P.D. 2003. You are what you eat: describing the foraging ecology of Southern elephant seals (Mirounga leonina) using blubber fatty acids. Proc. R. Soc. Lond. B. 270, 1283–1292.

    Article  Google Scholar 

  • Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., and Holmes, S.P. 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casaux, R., Baroni, A., and Carlini, A. 1997. The diet of the Weddell seal Leptonychotes weddelli at Harmony Point, South Shetland Islands. Polar Biol. 18, 371–375.

    Article  Google Scholar 

  • Castaner, O., Goday, A., Park, Y.M., Lee, S.H., Magkos, F., Shiow, S.A.T.E., and Schröder, H. 2018. The gut microbiome profile in obesity: a systematic review. Int. J. Endocrinol. 2018, 4095789.

    PubMed  PubMed Central  Google Scholar 

  • Clarke, K. and Gorley, R. 2006. PRIMER v6: user manual/tutorial (Plymouth Routines in Multivariate Ecological Research). PRIMER-E, Plymouth.

    Google Scholar 

  • David, L.A., Maurice, C.F., Carmody, R.N., Gootenberg, D.B., Button, J.E., Wolfe, B.E., Ling, A.V., Devlin, A.S., Varma, Y., Fischbach, M.A., et al. 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563.

    Article  CAS  PubMed  Google Scholar 

  • Delsuc, F., Metcalf, J.L., Wegener Parfrey, L., Song, S.J., González, A., and Knight, R. 2014. Convergence of gut microbiomes in myrmecophagous mammals. Mol. Ecol. 23, 1301–1317.

    Article  CAS  PubMed  Google Scholar 

  • Douglas, G.M., Maffei, V.J., Zaneveld, J.R., Yurgel, S.N., Brown, J.R., Taylor, C.M., Huttenhower, C., and Langille, M.G.I. 2020. PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol. 38, 685–688.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ducklow, H.W., Baker, K., Martinson, D.G., Quetin, L.B., Ross, R.M., Smith, R.C., Stammerjohn, S.E., Vernet, M., and Fraser, W. 2007. Marine pelagic ecosystems: the west Antarctic Peninsula. Phil. Trans. R. Soc. B 362, 67–94.

    Article  PubMed  Google Scholar 

  • Duncan, S.H., Belenguer, A., Holtrop, G., Johnstone, A.M., Flint, H.J., and Lobley, G.E. 2007. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl. Environ. Microbiol. 73, 1073–1078.

    Article  CAS  PubMed  Google Scholar 

  • Fadrosh, D.W., Ma, B., Gajer, P., Sengamalay, N., Ott, S., Brotman, R.M., and Ravel, J. 2014. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2, 6.

    Article  PubMed  PubMed Central  Google Scholar 

  • Favier, C.F., de Vos, W.M., and Akkermans, A.D.L. 2003. Development of bacterial and bifidobacterial communities in feces of newborn babies. Anaerobe 9, 219–229.

    Article  PubMed  Google Scholar 

  • Fearnbach, H., Durban, J.W., Ellifrit, D.K., and Pitman, R.L. 2019. Abundance of Type A killer whales (Orcinus orca) in the coastal waters off the western Antarctic Peninsula. Polar Biol. 42, 1477–1488.

    Article  Google Scholar 

  • Fernandes, A.D., Reid, J.N.S., Macklaim, J.M., McMurrough, T.A., Edgell, D.R., and Gloor, G.B. 2014. Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis. Microbiome 2, 15.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fierer, N., Jackson, J.A., Vilgalys, R., and Jackson, R.B. 2005. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl. Environ. Microbiol. 71, 4117–4120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Godon, J.J., Arulazhagan, P., Steyer, J.P., and Hamelin, J. 2016. Vertebrate bacterial gut diversity: size also matters. BMC Ecol. 16, 12.

    Article  PubMed  PubMed Central  Google Scholar 

  • Goetz, K.T., Burns, J.M., Hückstadt, L.A., Shero, M.R., and Costa, D.P. 2017. Temporal variation in isotopic composition and diet of Weddell seals in the western Ross Sea. Deep Sea Res. 2 Top. Stud. Oceanogr. 140, 36–44.

    Article  CAS  Google Scholar 

  • Green, K. and Burton, H.R. 1987. Seasonal and geographical variation in the food of Weddell seals, Leptonychotes weddelii, in Antarctica. Wildl. Res. 14, 475–489.

    Article  Google Scholar 

  • Groussin, M., Mazel, F., and Alm, E.J. 2020. Co-evolution and cospeciation of host-gut bacteria systems. Cell Host Microbe 28, 12–22.

    Article  CAS  PubMed  Google Scholar 

  • Hsieh, T.C., Ma, K.H., and Chao, A. 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol. Evol. 7, 1451–1456.

    Article  Google Scholar 

  • Kim, M. and Chun, J. 2014. 16S rRNA gene-based identification of Bacteria and Archaea using the EzTaxon server. Methods Microbiol. 41, 61–74.

    Article  CAS  Google Scholar 

  • Kim, M., Lim, H.S., Hyun, C.U., Cho, A., Noh, H.J., Hong, S.G., and Kim, O.S. 2019. Local-scale variation of soil bacterial communities in ice-free regions of maritime Antarctica. Soil Biol. Biochem. 133, 165–173.

    Article  CAS  Google Scholar 

  • Kinross, J.M., Darzi, A.W., and Nicholson, J.K. 2011. Gut microbiomehost interactions in health and disease. Genome Med. 3, 14.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lake, S., Burton, H., and Hoff, J. 2003. Regional, temporal and finescale spatial variation in Weddell seal diet at four coastal locations in east Antarctica. Mar. Ecol. Prog. Ser. 254, 293–305.

    Article  Google Scholar 

  • Leotta, G.A., Piñeyro, P., Serena, S., and Vigo, G.B. 2009. Prevalence of Edwardsiella tarda in Antarctic wildlife. Polar Biol. 32, 809–812.

    Article  Google Scholar 

  • Leser, T.D. and Mølbak, L. 2009. Better living through microbial action: the benefits of the mammalian gastrointestinal microbiota on the host. Environ. Microbiol. 11, 2194–2206.

    Article  CAS  PubMed  Google Scholar 

  • Lewis, R., O’Connell, T.C., Lewis, M., Campagna, C., and Hoelzel, A.R. 2006. Sex-specific foraging strategies and resource partitioning in the Southern elephant seal (Mirounga leonina). Proc. R. Soc. B 273, 2901–2907.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ley, R.E., Hamady, M., Lozupone, C., Turnbaugh, P.J., Ramey, R.R., Bircher, J.S., Schlegel, M.L., Tucker, T.A., Schrenzel, M.D., Knight, R., et al. 2008. Evolution of mammals and their gut microbes. Science 320, 1647–1651.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ley, R.E., Peterson, D.A., and Gordon, J.I. 2006a. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124, 837–848.

    Article  CAS  PubMed  Google Scholar 

  • Ley, R.E., Turnbaugh, P.J., Klein, S., and Gordon, J.I. 2006b. Human gut microbes associated with obesity. Nature 444, 1022–1023.

    Article  CAS  PubMed  Google Scholar 

  • Lozupone, C.A., Stombaugh, J.I., Gordon, J.I., Jansson, J.K., and Knight, R. 2012. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Madrid-Gambin, F., Oller-Moreno, S., Fernandez, L., Bartova, S., Giner, M.P., Joyce, C., Ferraro, F., Montoliu, I., Moco, S., and Marco, S. 2020. AlpsNMR: an R package for signal processing of fully untargeted NMR-based metabolomics. Bioinformatics 36, 2943–2945.

    Article  PubMed  Google Scholar 

  • Markle, J.G. and Fish, E.N. 2014. SeXX matters in immunity. Trends Immunol. 35, 97–104.

    Article  CAS  PubMed  Google Scholar 

  • Markle, J.G.M., Frank, D.N., Mortin-Toth, S., Robertson, C.E., Feazel, L.M., Rolle-Kampczyk, U., von Bergen, M., McCoy, K.D., Macpherson, A.J., and Danska, J.S. 2013. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339, 1084–1088.

    Article  CAS  PubMed  Google Scholar 

  • Martin, M. 2011. Cutadapt removes adapter sequences from highthroughput sequencing reads. EMBnet. J. 17, 10–12.

    Article  Google Scholar 

  • Min, Y., Ma, X., Sankaran, K., Ru, Y., Chen, L., Baiocchi, M., and Zhu, S. 2019. Sex-specific association between gut microbiome and fat distribution. Nat. Commun. 10, 2408.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Modig, A.O. 1996. Effects of body size and harem size on male reproductive behaviour in the southern elephant seal. Anim. Behav. 51, 1295–1306.

    Article  Google Scholar 

  • Moran, N.A. 2006. Symbiosis. Curr. Biol. 16, R866–R871.

    Article  CAS  PubMed  Google Scholar 

  • Muegge, B.D., Kuczynski, J., Knights, D., Clemente, J.C., González, A., Fontana, L., Henrissat, B., Knight, R., and Gordon, J.I. 2011. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970–974.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson, T.M., Apprill, A., Mann, J., Rogers, T.L., and Brown, M.V. 2015. The marine mammal microbiome: current knowledge and future directions. Microbiol. Aust. 36, 8–13.

    Article  Google Scholar 

  • Nelson, T.M., Rogers, T.L., and Brown, M.V. 2014. The gut bacterial community of mammals from marine and terrestrial habitats. PLoS ONE 8, e83655.

    Article  CAS  Google Scholar 

  • Nelson, T.M., Rogers, T.L., Carlini, A.R., and Brown, M.V. 2013. Diet and phylogeny shape the gut microbiota of Antarctic seals: a comparison of wild and captive animals. Environ. Microbiol. 15, 1132–1145.

    Article  CAS  PubMed  Google Scholar 

  • Ochman, H., Worobey, M., Kuo, C.H., Ndjango, J.B.N., Peeters, M., Hahn, B.H., and Hugenholtz, P. 2010. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol. 8, e1000546.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olsen, I. 2014. The family fusobacteriaceae. In Rosenberg, E., De-Long, E.F., Stackebrandt, E., and Thompson, F. (eds.), The Prokaryotes, pp. 109–132. Springer, Berlin, Heidelberg, Germany.

    Google Scholar 

  • Pacheco-Sandoval, A., Schramm, Y., Heckel, G., Brassea-Pérez, E., Martínez-Porchas, M., and Lago-Lestón, A. 2019. The Pacific harbor seal gut microbiota in Mexico: Its relationship with diet and functional inferences. PLoS ONE 14, e0221770.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park, S.B., Aoki, T., and Jung, T.S. 2012. Pathogenesis of and strategies for preventing Edwardsiella tarda infection in fish. Vet. Res. 43, 67.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pérez-Silva, J.G., Araujo-Voces, M., and Quesada, V. 2018. nVenn: generalized, quasi-proportional Venn and Euler diagrams. Bioinformatics 34, 2322–2324.

    Article  CAS  PubMed  Google Scholar 

  • Rooks, M.G. and Garrett, W.S. 2016. Gut microbiota, metabolites and host immunity. Nat. Rev. Immunol. 16, 341–352.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanders, J.G., Beichman, A.C., Roman, J., Scott, J.J., Emerson, D., Mc-Carthy, J.J., and Girguis, P.R. 2015. Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores. Nat. Commun. 6, 8285.

    Article  CAS  PubMed  Google Scholar 

  • Staniland, I.J., Ratcliffe, N., Trathan, P.N., and Forcada, J. 2018. Long term movements and activity patterns of an Antarctic marine apex predator: the leopard seal. PLoS ONE 13, e0197767.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stirling, I. 1969. Ecology of the Weddell seal in McMurdo sound, Antarctica. Ecology 50, 573–586.

    Article  Google Scholar 

  • Stoffel, M.A., Acevedo-Whitehouse, K., Morales-Durán, N., Grosser, S., Chakarov, N., Krüger, O., Nichols, H.J., Elorriaga-Verplancken, F.R., and Hoffman, J.I. 2020. Early sexual dimorphism in the developing gut microbiome of Northern elephant seals. Mol. Ecol. 29, 2109–2122.

    Article  PubMed  Google Scholar 

  • Tarnawski, B.A., Cassini, G.H., and Flores, D.A. 2013. Skull allometry and sexual dimorphism in the ontogeny of the Southern elephant seal (Mirounga leonina). Can. J. Zool. 92, 19–31.

    Article  Google Scholar 

  • The Human Microbiome Project Consortium. 2012. Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214.

    Article  CAS  PubMed Central  Google Scholar 

  • Yoon, S.H., Ha, S.M., Kwon, S., Lim, J., Kim, Y., Seo, H., and Chun, J. 2017. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int. J. Syst. Evol. Microbiol. 67, 1613–1617.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Youngblut, N.D., Reischer, G.H., Walters, W., Schuster, N., Walzer, C., Stalder, G., Ley, R.E., and Farnleitner, A.H. 2019. Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat. Commun. 10, 2200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This research was funded by Korea Polar Research Institute (PE20110). We are grateful to Dr. Min-Su Jeong for the help in the field. We thank to overwinter crews at King Sejong Station for logistic help. All the sampling protocols were approved from the Korean Ministry of Foreign Affairs and Trade and according to the current laws of the Republic of Korea (‘Act on Antarctic Activities and Protection of Antarctic Environment’).

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  1. Division of Polar Life Sciences, Korea Polar Research Institute, Incheon, 21990, Republic of Korea

    Mincheol Kim, Hyunjun Cho & Won Young Lee

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Correspondence to Won Young Lee.

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Kim, M., Cho, H. & Lee, W.Y. Distinct gut microbiotas between southern elephant seals and Weddell seals of Antarctica. J Microbiol. 58, 1018–1026 (2020). https://doi.org/10.1007/s12275-020-0524-3

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