Abstract
A comparative analysis of the intestinal microbiomes of some representatives of the Lake Baikal endemic family Comephoridae—the big oilfish Comephorus baicalensis (Pallas, 1776) and the little oilfish C. dybowski (Korotneff, 1904)—has been performed for the first time. The phylotype Akkermansia (phylum Verrucomicrobia) was detected in the C. dybowski microbiome, while Alistipes, Bacteroides, Chryseobacterium, Prevotella (Bacteroidetes), and Peptoniphilus (Firmicutes), were found in the C. baicalensis microbiome. Their presence in the intestine is associated with an elevated lipid uptake or an increase in the human and animal body weight. It is hypothesized that these microorganisms are involved in the lipid metabolism of the oilfish and determine their morphophysiological adaptations to pelagic life.
Similar content being viewed by others
References
Boutin, S., Sauvage, C., Bernatchez, L., Audet, C., and Derome, N., Inter individual variations of the fish skin microbiota: host genetics basis of mutualism?, PLoS One, 2014, vol. 9, no. 7, p. 102649.
Brahe, L.K., Le Chatelier, E., Prifti, E., Pons, N., Kennedy, S., Hansen, T., Pedersen, O., Astrup, A., Ehrlich, S.D., and Larsen, L.H., Specific gut microbiota features and metabolic markers in postmenopausal women with obesity, Nutr. Diab., 2015, vol. 5, p. 159.
Bridger, N., Walkty, A., Crockett, M., Fanella, S., Nichol, K., and Karlowsky, J.A., Caulobacter species as a cause of postneurosurgical bacterial meningitis in a pediatric patient, Can. J. Infect. Dis. Med. Microbiol., 2012, vol. 23, no. 1, pp. 10–12.
Carten, J.D., Bradford, M.K., and Farber, S.A., Visualizing digestive organ morphology and function using differential fatty acid metabolism in live zebrafish, Dev. Biol., 2011, vol. 360, pp. 276–285.
Le Chatelier, E., Nielsen, T., Qin, J., Prifti, E., Hildebrand, F., Falony, G., Almeida, M., Arumugam, M., Batto, J.M., Kennedy, S., Leonard, P., Li, J., Burgdorf, K., Grarup, N., Jørgensen, T., Brandslund, I., Nielsen, H.B., Juncker, A.S., Bertalan, M., Levenez, F., Pons, N., Rasmussen, S., Sunagawa, S., Tap, J., Tims, S., Zoetendal, E.G., Brunak, S., Clément, K., Doré, J., Kleerebezem, M., Kristiansen, K., Renault, P., Sicheritz-Ponten, T., de Vos, W.M., Zucker, J.D., Raes, J., Hansen, T., Guedon, E., Delorme, C., Layec, S., Khaci, G., van de Guchte, M., Vandemeulebrouck, G., Jamet, A., Dervyn, R., Sanchez, N., Maguin, E., Haimet, F., Winogradski, Y., Cultrone, A., Leclerc, M., Juste, C., Blottièrel, H., Pelletier, E., LePaslier, D., Artiguenave, F., Bruls, T., Weissenbach, J., Turner, K., Parkhill, J., Antolin, M., Manichanh, C., Casellas, F., Boruel, N., Varela, E., Torrejon, A., Guarner, F., Denariaz, G., Derrien, M., van Hylckama Vlieg, J.E.T., Veiga, P., Oozeer, R., Knol, J., Rescigno, M., Brechot, C., M’Rini, C., Merrieux, A., Yamada, T., Bork, P., Wang, J., Ehrlich, S.D., and Pedersen, O., Richness of human gut microbiome correlates with metabolic markers, Nature, 2013, vol. 500, pp. 541–546.
Cole, J.R., Wang, Q., Fish, J.A., Chai, B., McGarrell, D.M., Sun, Y., Brown, C.T., Porras-Alfaro, A., Kuske, C.R., and Tiedje, J.M., Ribosomal database project: data and tools for high throughput rRNA analysis, Nucleic Acids Res., 2014, database iss. 42, pp. 633–642.
Collado, M.C., Derrien, M., Isolauri, E., de Vos, W.M., and Salminen, S., Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly, Appl. Environ. Microbiol., 2007, vol. 73, pp. 7767–7770.
Cordero, H., Guardiola, F.A., Tapia-Paniagua, S.T., Cuesta, A., Meseguer, J., Balebona, M.C., Morinigo, M.A., and Esteban, M.A., Modulation of immunity and gut microbiota after dietary administration of alginate encapsulated Shewanella putrefaciens Pdp11 to gilthead seabream (Sparus aurata L.), Fish Shellfish Immunol., 2015, vol. 45, no. 2, pp. 608–618.
Dao, M.C., Everard, A., Aron-Wisnewsky, J., Sokolovska, N., Prifti, E., Verger, E.O., Kayser, B.D., Levenez, F., Chilloux, J., Hoyles, L., Le Mouhaër, S., Cotillard, A., Kennedy, S.P., Pons, N., Le Chatelier, E., Almeida, M., Quinquis, B., Galleron, N., Batto, J.-M., Renault, P., Zucker, J.-D., Dusko, Ehrlich S., Blottière, H., Leclerc, M., Juste, C., de Wouters, T., Lepage, P., Dumas, M.E., Rizkalla, S.W., Doré, J., Cani, P.D., and Clément, K., Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology, Gut, 2015. doi 10.1136/gutjnl-2014-308778
Derrien, M., Vaughan, E.E., Plugge, C.M., and de Vos, W.M., Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium, Int. J. Syst. Evol. Microbiol., 2004, vol. 54, pp. 1469–1476.
Derrien, M., Van Baarlen, P., Hooiveld, G., Norin, E., Müller, M., and de Vos, W.M., Modulation of mucosal immune response, tolerance, and proliferation in mice colonized by the mucin-degrader Akkermansia muciniphila, Front. Microbiol., 2011, vol. 2, pp. 1–14.
Franchini, P., Fruciano, C., Frickey, T., Jones, J.C., and Meyer, A., The gut microbial community of Midas cichlid fish in repeatedly evolved limnetic-benthic species pairs, PLoS One, 2014, vol. 9, no. 4, p. 95027.
Guinane, C.M. and Cotter, P.D., Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ, Ther. Adv. Gastroenterol., 2013, vol. 6, no. 4, pp. 295–308.
Hedberg, M.E., Israelsson, A., Moore, E.R., Svensson-Stadler, L., Wai, S.N., Pietz, G., Sandstrom, O., Hernell, O., Hammarström, M.L., and Hammarström, S., Prevotella jejuni sp. nov., isolated from the small intestine of a child with coeliac disease, Int. J. Syst. Evol. Microbiol., 2013, vol. 63, pp. 4218–4223.
Hu, X., Yu, J., Wang, C., and Chen, H., Cellulolytic bacteria associated with the gut of Dendroctonus armandi larvae (Coleoptera: Curculionidae: Scolytinae), Forests, 2014, vol. 5, pp. 455–465.
Hugon, P., Ramasamy, D., Lagier, J.C., Rivet, R., Couderc, C., Raoult, D., and Fournier, P.E., Non contiguousfinished genome sequence and description of Alistipes obesi sp. nov., Stand. Genomic Sci., 2013, vol. 7, no. 3, pp. 427–439.
Ingerslev, H.-C., von Gersdorff Jørgensen, L., Strube, M.L., Larsen, N., Dalsgaard, I., Boye, M., and Madsen, L., The development of the gut microbiota in rainbow trout (Oncorhynchus mykiss) is affected by first feeding and diet type, Aquaculture, 2014, vols. 424–425, pp. 24–34.
King, G.M., Judd, C., Kuske, C.R., and Smith, C., Analysis of stomach and gut microbiomes of the eastern oyster (Crassostrea virginica) from coastal Louisiana, USA, PLoS One, 2012, vol. 7, no. 12, p. 51475.
Kormas, K.A., Meziti, A., Mente, E., and Frentzos, A., Dietary differences are reflected on the gut prokaryotic community structure of wild and commercially reared sea bream (Sparus aurata), Microbiology Open, 2014, vol. 3, no. 5, pp. 718–728.
Koryakov, E.A., Pelagicheskie bychkovye Baikala (Pelagic Cottoidei of Lake Baikal), Moscow: Nauka, 1972.
Kostic, A.D., Howitt, M.R., and Garrett, W.S., Exploring host-microbiota interactions in animal models and humans, Genes Dev., 2013, vol. 27, no. 7, pp. 701–718.
Kozlova, T.A., and Khotimchenko, S.V., Lipids and fatty acids of two pelagic cottoid fishes (Comephorus spp.) endemic to Lake Baikal, Comp. Biochem. Physiol. Pt B: Biochem. Mol. Biol., 2000, vol. 127, pp. 477–485.
Larsen, A.M., Mohammed, H.H., and Arias, C.R., Characterization of the gut microbiota of three commercially valuable warmwater fish species, J. Appl. Microbiol., 2014, vol. 116, no. 6, pp. 1396–1404.
Leonard, A.B., Carlson, J.M., Bishoff, D.E., Sendelbach, S.I., Yung, S.B., Ramzanali, S., Manage, A.B.W., Hyde, E.R., Petrosino, J.F., and Primm, T.P., The skin microbiome of Gambusia affinis is defined and selective, Adv. Microbiol., 2014, vol. 4, pp. 335–343.
Li, X.M., Zhu, Y.J., Yan, Q.Y., Ringo, E., and Yang, D.G., Do the intestinal microbiotas differ between paddlefish (Polyodon spathala) and bighead carp (Aristichthys nobilis) reared in the same pond?, J. Appl. Microbiol., 2014, vol. 117, no. 5, pp. 1245–1252.
Lobo, C., Moreno-Ventas, X., Tapia-Paniagua, S., Rodriguez, C., Morinigo, M.A., and de La Banda, I.G., Dietary probiotic supplementation (Shewanella putrefaciens Pdp11) modulates gut microbiota and promotes growth and condition in Senegalese sole larviculture, Fish Physiol. Biochem., 2014, vol. 40, pp. 295–309.
Lukovac, S., Belzer, C., Pellis, L., Keijser, B.J., de Vos, W.M., Montijn, R.C., and Roeselers, G., Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids, MBio, 2014, vol. 5, no. 4, p. 01438–14.
Mishra, A.K., Hugon, P., Lagier, J.C., Nguyen, T.T., Robert, C., Couderc, C., Raoult, D., and Fournier, P.E., Non contiguous-finished genome sequence and description of Peptoniphilus obesi sp. nov., Stand. Genomic Sci., 2013, vol. 7, no. 3, pp. 357–369.
Moreno-Indias, I., Cardona, F., Tinahones, F.J., and Queipo-Ortuño, M.I., Impact of the gut microbiota on the development of obesity and type 2 diabetes mellitus, Front. Microbiol., 2014, vol. 5, art. 190, pp. 1–10.
Musso, G., Gambino, R., and Cassader, M., Obesity, diabetes, and gut microbiota. The hygiene hypothesis expanded?, Diab. Care, 2010, vol. 33, no. 10, pp. 2277–2284.
Rautio, M., Eerola, E., Väisänen-Tunkelrott, M.L., Molitoris, D., Lawson, P., Collins, M.D., and Jousimies-Somer, H., Reclassification of Bacteroides putredinis (Weinberg et al., 1937) in a new genus Alistipes gen. nov., as Alistipes putredinis comb. nov., and description of Alistipes finegoldii sp. nov., from human sources, Syst. Appl. Microbiol., 2003, vol. 26, no. 2, pp. 182–188.
Roeselers, G., Mittge, E.K., Stephens, W.Z., Parichy, D.M., Cavanaugh, C.M., Guillemin, K., and Rawls, J.F., Evidence for a core gut microbiota in the zebrafish, ISME J., 2011, vol. 5, no. 10, pp. 1595–1608.
Ryan, M.P., and Adley, C.C., Sphingomonas paucimobilis: a persistent gram-negative nosocomial infectious organism, J. Hosp. Infect., 2010, vol. 75, no. 3, pp. 153–157.
Semova, I., Carten, J.D., Stombaugh, J., Mackey, L.C., Knight, R., Farber, S.A., and Rawls, J.F., Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish, Cell Host Microbe, 2012, vol. 12, no. 3, pp. 277–288.
Sideleva, V.G., and Kozlova, T.A., Comparative study of endemic cottoid fish (Cottidae, Comephoridae) in relation to their adaptation to life in the pelagic zone of Lake Baikal, ZIN RAN, 2010, vol. 314, no. 4, pp. 433–447.
Starikov, G.V., Golomyanki Baikala (Baikal Oilfish), Novosibirsk: Nauka, 1977.
Taliev, D.N., Bychki-podkamenshchiki Baikala (Baikal Sculpins), Moscow: Izd. AN SSSR, 1955.
Wang, Q., Garrity, G.M., Tiedje, J.M., Cole, J.R., and Bayesian, N., Classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy, Appl. Environ. Microbiol., 2007, vol. 73, no. 16, pp. 5261–5267.
Zhang, H., DiBaise, J.K., Zuccolo, A., Kudrna, D., Braidottic, M., Yuc, Y., Parameswarana, P., Crowell, M.D., Wing, R., Rittmanna, B.E., and Krajmalnik-Browna, R., Human gut microbiota in obesity and after gastric bypass, Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, no. 7, pp. 2365–2370.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © E.V. Dzyuba, N.L. Bel’kova, N.N. Denikina, 2016, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2016, No. 6, pp. 658–662.
Rights and permissions
About this article
Cite this article
Dzyuba, E.V., Bel’kova, N.L. & Denikina, N.N. A study of the intestinal microbiomes of the Lake Baikal oilfishes (Cottoidei, Comephoridae). Biol Bull Russ Acad Sci 43, 573–577 (2016). https://doi.org/10.1134/S106235901606008X
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S106235901606008X