Microbial Communities Associated with the White Sea Red Algae as a Source of Xylanolytic Microorganisms

V. D. Salova; Салова В. Д.; A. M. Kholdina; Холдина А. М.; A. D. Mel’nik; Мельник А. Д.; K. S. Zayulina; Заюлина К. С.; A. G. El’cheninov; Ельченинов А. Г.; A. A. Klyukina; Клюкина А. А.; I. V. Kublanov; Кубланов И. В.

doi:10.31857/S0026365622600882

Microbial Communities Associated with the White Sea Red Algae as a Source of Xylanolytic Microorganisms

Authors: Salova V.D.¹, Kholdina A.M.¹, Mel’nik A.D.¹, Zayulina K.S.², El’cheninov A.G.², Klyukina A.A.², Kublanov I.V.¹^,2
Affiliations:
1. Faculty of Biology, Moscow State University
2. Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences
Issue: Vol 92, No 3 (2023)
Pages: 300-309
Section: ЭКСПЕРИМЕНТАЛЬНЫЕ СТАТЬИ
URL: https://journals.rcsi.science/0026-3656/article/view/138220
DOI: https://doi.org/10.31857/S0026365622600882
EDN: https://elibrary.ru/FXDEOK
ID: 138220

Cite item

Full Text

Open Access
Restricted Access

Access granted
Restricted Access

Subscription Access

Abstract
About the authors
References
Supplementary files
Statistics

Abstract

—Microorganisms associated with algae and able to utilize complex substrates (e.g., plant heteropolysaccharides) may be important producers of hydrolytic enzymes. The microbial communities of the red algae Corallina sp. and Phyllophora sp. sampled in the Kandalaksha Gulf basin of the White Sea were analyzed using high-throughput sequencing of the V4-variable region of the 16S rRNA gene. The dominant phyla in microbiomes of both samples were Pseudomonadota and Bacteroidota (GTDB classification, https://gtdb.ecogenomic.org/). For the Corallina sp. sample, dominance of the Vibrio, Agarivorans, and Photobacterium genera was shown, while Granulosicoccus and Aliivibrio dominated in the Phyllophora sp. sample. The analyzed red macroalgae with associated microbiota were used as an inocula to obtain microbial enrichment cultures growing on β-1,4-xylan or β-1,3-glucan (сurdlan). It was shown that, similar to environmental samples Pseudomonadota and Bacteroidota phyla representatives were prevalent in all enrichment cultures. However, unlike the environmental samples, in the enrichment cultures the dominant genera were Marinomonas, Reinekea, Polaribacter, and Pseudoalteromonas. The latter, as well as the representatives of Vibrio sp., were isolated in pure cultures for which the xylanolytic activity was shown.

Keywords

White Sea, red algae, microbial diversity, high-throughput sequencing, 16S rRNA gene, xylanolytic microorganisms

References

Горленко В.М., Пучкова Н.Н., Демчев В.В. Фотосинтезирующие микроорганизмы супралиторали Белого моря // Биологические науки. 1985. Т. 5. С. 66‒72.
Заварзин Г.А. Становление биосферы // Микробиология. 1997. Т. 66. С. 725‒734.
Zavarzin G.A. The rise of the biosphere // Microbiology (Moscow). 1997. V. 66. P. 603‒611.
Кравчишина М.Д., Мицкевич И.Н., Веслополова Е.Ф., Шевченко В.П., Лисицын А.П. Взаимосвязь взвеси и микроорганизмов в водах Белого моря // Океанология. 2008. Т. 48. С. 900‒917.
Kravchishina M.D., Mitzkevich I.N., Veslopolova E.F., Shevchenko V.P., Lisitzin A.P. Relationship between the suspended particulate matter and microorganisms in the White Sea waters // Oceanology. 2008. V. 48. P. 837‒854.
Романкевич Е.А., Ветров А.А. Цикл углерода в арктических морях России. М.: Наука, 2001. 300 с.
Саввичев А.С., Русанов И.И., Захарова Е.Е., Веслополова Е.Ф., Мицкевич И.Н., Кравчишина М.Д., Леин А.Ю., Иванов М.В. Микробные процессы циклов углерода и серы в Белом море // Микробиология. 2008. Т. 77. С. 823‒838.
Savvichev A.S., Rusanov I.I., Zakharova E.E., Veslopolova E.F., Mitskevich I.N., Kravchishina M.D., Lein A.Yu., Ivanov M.V. Microbial processes of the carbon and sulfur cycles in the White Sea // Microbiology (Moscow) 2008. V. 77. P. 734‒750.
Саввичев А.С., Русанов И.И., Юсупов С.К., Байрамов И.Т., Пименов Н.В., Леин А.Ю., Иванов М.В. Процесс микробной сульфатредукции в осадках прибрежной зоны и литорали Кандалакшского залива Белого моря // Микробиология. 2003. Т. 72. С. 535‒546.
Savvichev A.S., Rusanov I.I., Yusupov S.K., Bairamov I.T., Pimenov N.V., Lein A.Y., Ivanov M.V. The process of microbial sulfate reduction in sediments of the coastal zone and littoral of the Kandalaksha Bay of the White Sea // Microbiology (Moscow). 2003. V. 72. P. 478–489.
Семенова Е.В., Шлыкова Д.С., Семенов А.М., Иванов М.Н., Шеляков О.В., Нетрусов А.И. Бактерии-эпифиты бурых водорослей в утилизации нефти в экосистемах северных морей // Вестник Моск. ун-та. Сер. 16. Биология. 2009. № 3. С. 18‒22.
Чикин С.М., Тарасова Н.А., Саралов А.И., Банникова О.М. Особенности распространения бактерио- и мезозоопланктона в прибрежных водах Белого и Баренцева морей // Микробиология. 2003. Т. 72. С. 250‒258.
Chikin S.M., Tarasova N.A., Saralov A.I., Bannikova O.M. The distribution of bacterio- and mesozooplankton in the coastal waters of the White and Barents seas // Microbiology (Moscow). 2003. V. 72. P. 213‒220.
Araki T., Tani S., Maeda K., Hashikawa S., Nakagawa H., Morishita T. Purification and characterization of β-1,3-xylanase from a marine bacterium, Vibrio sp. XY-214 // Bios-ci. Biotechnol. Biochem. 1999. V. 63. P. 2017‒2019.
Avcı B., Hahnke R.L., Chafee M., Fischer T., Gruber-Vodicka H., Tegetmeyer H.E., Harder J., Fuchs B.M., Amann R.I., Teeling H. Genomic and physiological analyses of ‘Reinekea forsetii’ reveal a versatile opportunistic lifestyle during spring algae blooms // Environ. Microbiol. 2017. V. 19. P. 1209‒1221.
Avcı B., Krüger K., Fuchs B.M., Teeling H., Amann R.I. Polysaccharide niche partitioning of distinct Polaribacter clades during North Sea spring algal blooms // ISME J. 2020. V. 14. № 6. P. 1369‒1383.
Bolyen E., Rideout J.R., Dillon M.R., Bokulich N.A., Abnet C.C., Al-Ghalith G.A., Alexander H., Alm E.J., Arumugam M., Asnicar F. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 // Nat. Biotechnol. 2019. V. 37. P. 852–857.
Brodie J., Williamson C., Barker G.L., Walker R.H., Briscoe A., Yallop M. Characterising the microbiome of Corallina officinalis, a dominant calcified intertidal red alga // FEMS Microbiol. Ecol. 2016. V. 92. P. fiw110.
Deniaud E., Quemener B., Fleurence J., Lahaye M. Structural studies of the mix-linked β-(1 → 3)/β-(1 → 4)-D-xylans from the cell wall of Palmaria palmata (Rhodophyta) // Int. J. Biol. Macromol. 2003. V. 33. P. 9‒18.
Ducklow H.W. Production and fate of bacteria in the oceans // Bioscience. 1983. V. 33. P. 494‒501.
Fisher R.A., Corbet A.S., Williams C.B. The relation between the number of species and the number of individuals in a random sample of an animal population // J. Anim. Ecol. 1943. V. 12. P. 42‒58.
Gaitan-Espitia J.D., Schmid M. Diversity and functioning of Antarctic seaweed microbiomes // Antarctic Seaweeds: Diversity, Adaptation and Ecosystem Services / Eds. Gómez I., Huovinen P. Cham: Springer, 2020. P. 279‒291.
Gavrilov S.N., Korzhenkov A.A., Kublanov I.V., Bargiela R., Zamana L.V., Popova A.A., Peter S.V., Golyshin N., Golyshina O.V. Microbial communities of polymetallic deposits’ acidic ecosystems of continental climatic zone with high temperature contrasts // Front. Microbiol. 2019. Art. 1573.
Gavrilov S.N., Stracke C., Jensen K., Menzel P., Kallnik V., Slesarev A., Sokolova T., Zayulina K., Brasen K., Bonch-Osmolovskaya E.A., Peng X., Kublanov I., Siebers B. Isolation and characterization of the first xylanolytic hyperthermophilic euryarchaeon Thermococcus sp. strain 2319X1 and its unusual multidomain glycosidase // Front. Microbiol. 2016. V. 7. Art. 552.
Gobet A., Barbeyron T., Matard-Mann M., Magdelenat G., Vallenet D., Duchaud E., Michel G. Evolutionary evidence of algal polysaccharide degradation acquisition by Pseudoalteromonas carrageenovora 9T to adapt to macroalgal niches // Front. Microbiol. 2018. V. 9. Art. 2740.
Gorrasi S., Pesciaroli C., Barghini P., Pasqualetti M., Fenice M. Structure and diversity of the bacterial community of an Arctic estuarine system (Kandalaksha Bay) subject to intense tidal currents // J. Mar. Syst. 2019a. V. 196. P. 77‒85.
Gorrasi S., Pesciaroli C., Barghini P., Pasqualetti M., Giovannini V., Massimiliano F. Metagenetic profiling of the bacterial communities of an intertidal pool in Kandalaksha Bay (White Sea, Russia) // J. Environ. Prot. Ecol. 2019b. V. 20. P. 1317‒1324.
Hollants J., Leliaert F., De Clerck O., Willems A. What we can learn from sushi: a review on seaweed–bacterial associations // FEMS Microbiol. Ecol. 2013. V. 83. P. 1‒16.
Hsieh Y.S.Y., Harris P.J. Xylans of red and green algae: what is known about their structures and how they are synthesised? // Polymers. 2019. V. 11. Art. 354.
Huggett M.J., Williamson J.E., De Nys R., Kjelleberg S., Steinberg P.D. Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae // Oecologia. 2006. V. 149. P. 604‒619.
Iriki Y., Suzuki T., Nisizawa K., Miwa T. Xylan of siphonaceous green algae // Nature. 1960. V. 87. P. 82‒83.
Johnson J., Sudheer P.D., Yang Y.H., Kim Y.G., Choi K.Y. Hydrolytic activities of hydrolase enzymes from halophilic microorganisms // Biotechnol. Bioproc. Eng. 2017. V. 22. P. 450‒461.
Kim S.J., Kim J.G., Lee S.H., Park S.J., Gwak J.H., Jung M.Y., Chung W.H., Yang E.J., Park J., Jung J., Hahn Y., Cho J.C., Madsen E.L., Rodriguez-Valera F., Hyun J.H., Rhee S.K. Genomic and metatranscriptomic analyses of carbon remineralization in an Antarctic polynya // Microbiome. 2019. V. 7. P. 1‒15.
Kloareg B., Quatrano R.S. Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides // Oceanography and Marine Biology: an Annual Review. 1988. V. 26. P. 259‒315.
Leliaert F., Smith D.R., Moreau H., Herron M.D., Verbruggen H., Delwiche C.F., Clerck O.D. Phylogeny and molecular evolution of the green algae // Crit. Rev. Plant Sci. 2012. V. 31. P. 1–46.
Mandal A. Review on microbial xylanases and their applications // Int. J. Life Sci. 2015. V. 4. P. 178‒187.
Martin M., Barbeyron T., Martin R., Portetelle D., Michel G., Vandenbol M. The cultivable surface microbiota of the brown alga Ascophyllum nodosum is enriched in macroalgal-polysaccharide-degrading bacteria // Front. Microbiol. 2015. V. 6. Art. 1487.
Pesciaroli C., Rodelas B., Juarez-Jiménez B., Barghini P., Fenice M. Bacterial community structure of a coastal area in Kandalaksha Bay, White Sea, Russia: possible relation to tidal hydrodynamics // Ann. Microbiol. 2015. V. 65. P. 443‒453.
Pielou E.C. The measurement of diversity in different types of biological collections // J. Theor. Biol. 1966. V. 13. P. 131‒144.
Qeshmi F.I., Homaei A., Fernandes P., Hemmati R., Dijkstra B.W., Khajeh K. Xylanases from marine microorganisms: a brief overview on scope, sources, features and potential applications // Biochim. Biophys. Acta ‒ Proteins Proteom. 2020. V. 1868. P. 140312.
Ray S., Vigouroux J., Bouder A., Allami M.F., Geairon A., Fanuel M., Ropartz D., Helbert W., Lahaye M., Bonnin E. Functional exploration of Pseudoalteromonas atlantica as a source of hemicellulose-active enzymes: evidence for a GH8 xylanase with unusual mode of action // Enzyme Microb. Technol. 2019. V. 127. P. 6‒16.
Shannon C.E., Weaver W. The Mathematical Theory of Communication. University of Illinois. Urbana, 1949. V. 117.
Shuvaeva G.P., Sysoeva M.G. Xylanase of the micromycete Rhizopus var. microsporus 595: preparation, structural and functional characteristics, and application // Appl. Biochem. Microbiol. 2010. V. 46. P. 641‒647.
Singh R.P., Reddy C.R.K. Seaweed–microbial interactions: key functions of seaweed-associated bacteria // FEMS Microbiol. Ecol. 2014. V. 88. P. 213‒230.
Sorensen T.A. A method of establishing groups of equal amplitude in plant sociology based on similarity of species content and its application to analyses of the vegetation on Danish commons // Biol. Skar. 1948. V. 5. P. 1‒34.
Suleiman M., Krüger A., Antranikian G. Biomass-degrading glycoside hydrolases of archaeal origin // Biotechnol. Biofuels. 2020. V. 13. P. 1‒14.
Trias R., García-Lledó A., Sánchez N., López-Jurado J.L., Hallin S., Bañeras L. Abundance and composition of epiphytic bacterial and archaeal ammonia oxidizers of marine red and brown macroalgae // Appl. Environ. Microbiol. 2012. V. 78. P. 318‒325.
Umemoto Y., Shibata T., Araki T. D-xylose isomerase from a marine bacterium, Vibrio sp. strain XY-214, and D-xylulose production from β-1,3-xylan // Mar. Biotechnol. 2012. V. 14. P. 10‒20.
Vortsepneva E., Chevaldonné P., Klyukina A., Naduvaeva E., Todt C., Zhadan A., Tzetlin A., Kublanov I. Microbial associations of shallow-water Mediterranean marine cave Solenogastres (Mollusca) // PeerJ. 2021. V. 9. P. e12655.
Xing P., Hahnke R.L., Unfried F., Markert S., Huang S., Barbeyron T., Harder J., Becher D., Schweder T., Glöckner F.O., Amann R.I., Teeling H. Niches of two polysaccharide-degrading Polaribacter isolates from the North Sea during a spring diatom bloom // ISME J. 2015. V. 9. P. 1410‒1422.
Yoon H.S., Nelson W., Lindtrom S.C., Boo S.M., Pueschel C., Qiu H., Bhattacharya D. Rhodophyta // Handbook of the Protists / Eds. Archibald J.M., Simpson A.G.B., Slamovits C.H. Cham: Springer, 2017a. P. 89–133.
Yoon K., Song J.Y., Kwak M.J., Kwon S.K., Kim J.F. Genome characteristics of the proteorhodopsin-containing marine flavobacterium Polaribacter dokdonensis DSW-5 // J. Microbiol. 2017b. V. 55. P. 561‒567.
Yu W.N., Du Z.Z., Chang Y.Q., Mu D.S., Du Z.J. Marinomonas agarivorans sp. nov., an agar-degrading marine bacterium isolated from red algae // Int. J. Syst. Evol. Microb-iol. 2020. V. 70. P. 100‒104.