doi: 10.15389/agrobiology.2020.4.697eng
UDC: 636.294:579.62:577.2
Acknowledgements:
Supported financially by Russian Science Foundation for project No. 17-76-20026 “Rumen microbiocenosis in Rangifer tarandus of the Russian Arctic as a fundamentals for promising animal biotechnologies”
VARIATION IN THE RUSSIAN ARCTIC REINDEER (Rangifer tarandus) RUMEN MICROBIOME RELATED TO SEASON CHANGE
L.A. Ilina1, V.A. Filippova1, K.A. Layshev2, E.A. Yildirim1,
T.P. Dunyashev1, E.A. Brazhnik1, A.V. Dubrovin1, D.V. Sobolev1,
D.G. Tiurina1, N.I. Novikova1, G.Yu. Laptev1, A.A. Yuzhakov2,
T.M. Romanenko3, Yu.P. Vylko3
1JSC Biotrof+, 19, korp. 1, Zagrebskii bulv., St. Petersburg, 192284 Russia, e-mail ilina@biotrof.ru (✉ corresponding author), deniz@biotrof.ru, filippova@biotrof.ru, timur@biotrof.ru, dubrowin.a.v@yandex.ru, sdv@biotrof.ru, natalia-iv-nov@rambler.ru, georg-laptev@rambler.ru;
2Northwest Center for Interdisciplinary Research of Food Security Problems, 7, sh. Podbel’skogo, St. Petersburg—Pushkin, 196608 Russia, e-mail layshev@mail.ru, alyuzhakov@mail.ru;
3Laverov Federal Center for Integrated Arctic Research (FCIARctic) RAS, Naryan-Mar Agro-Experimental Station, 1a, ul. Rybnikov, Naryan-Mar, Nenets AO, 166004 Russia, e-mail nmshos@atnet.ru, vylcko.yury@yandex.ru
ORCID:
Ilina L.A. orcid.org/0000-0003-2789-4844
Sobolev D.V. orcid.org/0000-0002-3238-979X
Laishev K.A. orcid.org/0000-0003-2490-6942
Novikova N.I. orcid.org/0000-0002-9647-4184
Yildirim E.A. orcid.org/0000-0002-5846-5105
Laptev G.Yu. orcid.org/0000-0002-8795-6659
Filippova V.A. orcid.org/0000-0001-8789-9837
Yuzhakov A.A. orcid.org/0000-0002-0633-4074
Dunyashev T.P. orcid.org/0000-0002-3918-0948
Romanenko Т.М. orcid.org/0000-0003-0034-7453
Dubrovin A.V. orcid.org/0000-0001-8424-4114
Vylko Yu.P. orcid.org/0000-0002-6168-8262
Received April 15, 2020
Reindeer (Rangifer tarandus) is a large Holarctic herbivore animal, the habitat of which, including its existence at low temperatures and poor diets, has led to the evolutionary development of their unique rumen microbiota, which is necessary for the efficient assimilation of the Arctic flora. In winter, lichens rich in secondary metabolites which can influence the representatives of the microbial consortium of the digestive tract, make up a large proportion of reindeer fodder plants. The toxic effects of certain lichen metabolites (e.g., usnic acid) on a number of microorganisms (Clostridiales, Enterococcus, Staphylococcus aureus, Escherichia coli, etc.) as well as ruminants (elk) were previously reported. However, little is known about the effect of lichen consumption on the reindeer rumen microbiome. Using molecular analysis, we were the first to study the seasonal patterns of the formation of the microbial communities of the rumen of the reindeer Rangifer tarandus, living in the Russian Arctic. The purpose of the study was to compare the composition of the bacterial community of the reindeer rumen in the summer-autumn and winter-spring periods using the method of NGS-sequencing. In the analysis of microbial communities, biodiversity, taxonomic structure, and the relationship of these indicators with the characteristics of reindeer nutrition in connection with seasonal changes were evaluated. Samples of the rumen content were collected in the summer-autumn and winter-spring periods in 2017-2018 from 20 Nenets reindeer (calves 4-8 months old and adult animals 3-6 years old, n = 3 per each age group) in the Nenets Autonomous District (AD). Seasonal differences, in contrast to gender and age, turned out to be the main factor influencing the reindeer rumen bacterial community, which, most likely, is due to differences in the composition of the pasture diet. In the summer-autumn period, a significant increase in the α-biodiversity of the rumen microbiome was noted compared to the winter-spring time for the number of OTUs, Chao1 and Shannon indices. A comparison of the β-diversity of the reindeer rumen microbiota composition has demonstrated the presence of pronounced cluster formation for samples collected in different seasons of the year. Despite the fact that in the winter period the diet of reindeer was mainly represented by lichens which are not typical food for other ruminants (such as cattle, sheep, etc.), it was interesting to note that, on the whole, the obtained microbiome profiles correspond to modern ideas about the ruminant rumen microbiota. Nevertheless, during different seasonal periods, significant changes in the representation of a number of taxa were noted, the clearest of which were detected for microorganisms associated with feed polysaccharide fermentation. So, in the winter-spring season, a significant increase in microorganisms that decompose polysaccharides of lichens, including hemicellulose (Butyrivibrio, Ruminococcus), and lichenin (Succiniclasticum, Paraprevotellaceae,and Prevotella). In the summer-autumn period, a significant increase in the proportion of cellulolytic bacteria (Clostridium, Blautia, Clostridiales, Christensenellaceae Mogibacteriaceae,and Prevotellaceae) is noted. In addition, it has been shown that in the summer period a whole spectrum of microorganisms that belong to bacterial pathogens, including Erysipelotrichaceae, Coriobacteriaceae, Mycoplasmataceae,and Rickettsiales, proliferate in the reindeer rumen. On the whole, the results obtained allow us to conclude that the reindeer rumen microbiome is quite clearly associated with nutritional characteristics during various seasonal periods, which determine adaptation to environmental conditions.
Keywords: Rangifer tarandus, reindeer, rumen, microbiome, seasonal changes, NGS, Russian Arctic.
REFERENCES
- Morgavi D.P., Kelly W.J., Janssen P.H., Attwood G.T. Rumen microbial (meta)genomics and its application to ruminant production. Animal, 2013, 7(1): 184-201 CrossRef
- Mathiesen S.D., Mackie R.I., Aschfalk A., Ringø E., Sundset M.A. Microbial ecology of the digestive tract in reindeer: seasonal changes. In: Biology of growing animals. Vol. 2 Microbial ecology in growing animals. W.H. Holzapfel, P.J. Naughton, S.G. Pierzynowski, R. Zabielski, E. Salek (eds.). Elsevier Ltd., Edinburgh, 2005: 75-102 CrossRef
- Aagnes T.H., Sørmo W., Mathiesen S.D. Ruminal microbial digestion in free living, in captive lichen-fed and in starved reindeer (Rangifer tarandus tarandus) in winter. Applied and Environmental Microbiology, 1995, 61(2): 583-591.
- Orpin C.G., Mathiesen S.D., Greenwood Y., Blix A.S. Seasonal changes in the ruminal microflora of the high-arctic Svalbard reindeer (Rangifer tarandus platyrhynchus). Applied and Environmental Microbiology, 1985, 50(1): 144-151.
- Sundset M.A., Kohn A., Mathiesen S.D., Praesteng K.E. Eubacterium rangiferina, a novel usnic acid-resistant bacterium from the reindeer rumen. Naturwissenschaften, 2008, 95(8): 741-749 CrossRef
- Kartsev V., Lichitsky B., Geronikaki A., Petrou A., Smiljkovic M., Kostic M., Radanovic O., Soković M. Design, synthesis and antimicrobial activity of usnic acid derivatives. Med. Chem. Commun., 2018, 9(5): 870-882 CrossRef
- Roach J.A.G., Musser S.M., Morehouse K., Woo J.Y.J. Determination of usnic acid in lichen toxic to elk by liquid chromatography with ultraviolet and tandem mass spectrometry determination. J. Agric. Food. Chem., 2006, 54(7): 2484-2490 CrossRef
- Dailey R.N, Montgomery D.L., Ingram J.T., Siemion R., Vasquez M., Raisbeck M.F. Toxicity of lichen secondary metabolite (+)-Usnic acid in domestic sheep. Veterinary Pathology, 2008, 45(1): 19-25 CrossRef
- Palo R.T. Usnic acid, a secondary metabolite of lichens and its effect on in vitro digestibility in reindeer. Rangifer, 1993, 13(1): 39-43 CrossRef
- Sundset M.A., Barboza P.S., Green T.K., Folkow L.P., Blix A.S., Mathiesen S.D. Microbial degradation of usnic acid in the reindeer rumen. Naturwissenschaften, 2010, 97: 273-278 CrossRef
- Henderson G., Cox F., Ganesh S., Jonker A., Young W., Global Rumen Census Collaborators, Janssen P.H. Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Scientific Reports, 2015, 5: 14567 CrossRef
- Fonty G., Joblin K., Chavarot M., Roux R., Naylor G., Michallon F. Establishment and development of ruminal hydrogenotrophs in methanogen-free lambs. Applied and Environmental Microbiology, 2007, 73(20): 6391-6403 CrossRef
- Sundset M.A., Præsteng K.E., Cann I.K.O., Mathiesen S.D., Mackie R.I. Novel rumen bacterial diversity in two geographically separated sub-species of reindeer. Microb. Ecol., 2007, 54(3): 424-438 CrossRef
- Crater A.R., Barboza P.S., Forster R. Regulation of rumen fermentation during seasonal fluctuations in food intake of muskoxen. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 2007, 146(2): 233-241 CrossRef
- Rustomo B., AlZahal O., Odongo N., Duffield T.F., McBride B.W. Effects of rumen acid load from feed and forage particle size on ruminal pH and dry matter intake in the lactating dairy cow. Journal of Dairy Science, 2006, 89(12): 4758-4768 CrossRef
- Kleen J.L., Hooijer G.A., Rehage J., Noordhuizen J.P. Subacute ruminal acidosis (SARA): a review. Journal of Veterinary Medicine Series A, 2003, 50(8): 406-414 CrossRef
- McEwan N.R., Abecia L., Regensbogenova M., Adam C.L., Findlay P.A., Newbold C.J. Rumen microbial population dynamics in response to photoperiod. Letters in Applied Microbiology, 2005, 41(1): 97-101 CrossRef
- Uyeno Y., Sekiguchi Y., Tajima K., Takenaka A., Kurihara M., Kamagata Y. An rRNA-based analysis for evaluating the effect of heat stress on the rumen microbial composition of Holstein heifers. Anaerobe, 2010, 16(1): 27-33 CrossRef
- Romero-Pérez G.A., Ominski K.H., McAllister T.A., Krause D.O. Effect of environmental factors and influence of rumen and hindgut biogeography on bacterial communities in steers. Applied and Environmental Microbiology, 2011, 77(1): 258-268 CrossRef
- Olsen M.A., Aagnes T.H., Mathiesen S.D. The effect of timothy silage on the bacterial population in rumen fluid of reindeer (Rangifer tarandus tarandus) from natural summer and winter pasture. FEMS Microbiology Ecology, 1997, 24(2): 127-136 CrossRef
- Wang T.Y., Chen H.L., Lu M.J., Chen Y.C., Sung H.M., Mao C.T., Cho H.Y., Ke H.M., Hwa T.Y., Ruan S.K., Hung K.Y., Chen C.K., Li J.Y., Wu Y.C., Chen Y.H., Chou S.P., Tsai Y.W., Chu T.C., Shih C.A., Li W.H., Shih M.C. Functional characterization of cellulases identified from the cow rumen fungus Neocallimastix patriciarum W5 by transcriptomic and secretomic analyses. Biotechnol. Biofuels, 2011, 4: 24 CrossRef
- Fonty G., Joblin K.N. Rumen anaerobic fungi: their role and interactions with other rumen microorganisms in relation to fiber digestion. In: Physiological aspects of digestion and metabolism in ruminants. Academic Press, Toronto, ON, 1990: 665-680.
- Sundset M.A., Edwards J.E., Cheng Y.F., Senosiain R.S., Fraile M.N., Northwood K.S., Præsteng K.E., Glad T., Mathiesen S.D., Wright A.D.G. Molecular diversity of the rumen microbiome of Norwegian reindeer on natural summer pasture. Microb. Ecol., 2009, 57(2): 335-348 CrossRef
- Sundset M.A., Edwards J.E., Cheng Y.F., Senosiain R.S., Fraile M.N., Northwood K.S., Praesteng K.E., Glad T., Mathiesen S.D., Wright A.D. Rumen microbial diversity in Svalbard reindeer, with particular emphasis on methanogenic archaea. FEMS Microbiology Ecology, 2009, 70(3): 553-562 CrossRef
- Salgado-Flores A., Hagen L.H., Ishaq S.L., Zamanzadeh M., Wright A.D.G., Pope P.B., Sundset M.A. Rumen and cecum microbiomes in reindeer (Rangifer tarandus tarandus) are changed in response to a lichen diet and may affect enteric methane emissions. PLoS ONE, 2016, 11(5): e0155213 CrossRef
- Polezhaev A.N., Berkutenko A.N. Opredelitel' kormovykh rastenii severnogo olenya: Magadanskaya oblast' [Keys to forage plants for reindeer: Magadan region]. Magadan, 1981 (in Russ.).
- Motovilov K.Ya., Bulatov A.P, Poznyakovskii P.M., Lantseva N.N., Mikolaichik I.N. Ekspertiza kormov i kormovykh dobavok [Expertise of feed and feed additives]. Novosibirsk, 2004 (in Russ.).
- Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Pesa A.G., Goodrich J.K., Gordon J.I., Huttley G.A., Kelley S.T., Knights D., Koenig J.E., Ley R.E., Lozupone C.A., McDonald D., Muegge B.D., Pirrung M., Reeder J., Sevinsky J.R., Turnbaugh P.J., Walters W.A., Widmann J., Yatsunenko T., Zaneveld J., Knight R. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 2010, 7: 335-336 CrossRef
- Oliveros J.C. Venny. An interactive tool for comparing lists with Venn’s diagrams. 2007. Accessed: http://bioinfogp.cnb.csic.es/tools/venny/index.html. No date.
- Warton D.I., Wright T.W., Wang Y. Distance-based multivariate analyses confound location and dispersion effects. Methods in Ecology and Evolution, 2012, 3(1): 89-101 CrossRef
- Morgavi D.P., Kelly W.J., Janssen P.H., Attwood G.T. Rumen microbial (meta)genomics and its application to ruminant production. Animal, 2013, 7(1): 184-201 CrossRef
- Person S.J., White R.G., Luick J.R. Determination of nutritive value of reindeer-caribou range, In: Proceedings of the 2nd International Reindeer and Caribou Symposium. E. Reimers, E. Gaare, S. Skjenneberg (eds.). Direktoratet for vilt og ferskvannsfisk, Trondheim, Norway, 1980: 224-239.
- Church D.C. Ruminant animal: digestive physiology and nutrition. Prentice Hall, New Jersey, 1993.
- Hungate R.E. The rumen and its microbes. Academic Press, NY, 1966.
- Hackmann T.J., Spain J.N. Invited review: ruminant ecology and evolution: perspectives useful to ruminant livestock research and production. Journal of Dairy Science, 2010, 93(4): 1320-1334 CrossRef
- Peng S., Yin J., Liu X., Jia B., Chang Z., Lu H., Jiang N., Chen Q. First insights into the microbial diversity in the omasum and reticulum of bovine using Illumina sequencing. J. Appl. Genetics, 2015, 56(3): 393-401 CrossRef
- Smith C.C.R., Snowberg L.K., Gregory C.J., Knight R., Bolnick D.I. Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota. ISME J., 2015, 9(11): 2515-2526 CrossRef
- Fiere N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nature Reviews Microbiology, 2017, 15: 579-590 CrossRef
- Shen J., Zheng L., Chen X., Han X., Cao Y., Yao J. Metagenomic analyses of microbial and carbohydrate-active enzymes in the rumen of dairy goats fed different rumen degradable starch. Frontiers in Microbiology, 2020, 11: 1003 CrossRef
- Li Z.P., Liu H.L., Guang Y.L., Bao K., Wang K.Y., Xu C., Yang Y.F., Yang H.F., Wright A.D.G. Molecular diversity of rumen bacterial communities from tannin-rich and fiber-rich forage fed domestic Sika deer (Cervus nippon) in China. BMC Microbiol., 2013, 13: 151 CrossRef
- Li F., Li C., Chen Y., Liu J. Host genetics influence the rumen microbiota and heritable rumen microbial features associate with feed efficiency in cattle. Microbiome, 2019, 7: 92 CrossRef
- Zielińska S., Kidawa D., Stempniewicz L., Łoś M., Łoś J.M. New insights into the microbiota of the Svalbard Reindeer Rangifer tarandus platyrhynchus. Frontiers in Microbiology, 2016, 7: 170 CrossRef
- Mathiesen S.D, Haga Ø.E, Kaino T., Tyler N.J.C. Diet composition, rumen papillation and maintenance of carcass mass in female Norwegian reindeer (Rangifer tarandus tarandus) in winter. Journal of Zoology, 2000, 251(1): 129-138 CrossRef
- Zhou M., Peng Y., Chen Y., Klinger C., Masahito O., Liu J., Guan L. Assessment of microbiome changes after rumen transfaunation: implications on improving feed efficiency in beef cattle. Microbiome, 2018, 6: 62 CrossRef
- Kazanovskii E.S., Karabanov V.P., Klebenson K.A. Bolezni severnykh olenei [Diseases in reindeer]. Syktyvkar, 2011 (in Russ.).
- Morita H., Shiratori C., Murakami M., Takami H., Toh H., Kato Y., Nakajima F., Takagi M., Akita H., Masaoka T., Hattori M. Sharpea azabuensis gen. nov., sp. nov., a Gram-positive, strictly anaerobic bacterium isolated from the faeces of thoroughbred horses. International Journal of Systematic and Evolutionary Microbiology, 2008, 58(12): 2682-2686 CrossRef
- Nocek J.E. Bovine acidosis: implications on laminitis. Journal of Dairy Science, 1997, 80: 1005-1028 CrossRef