Chitin Degradation by Microbial Communities of the Kandalaksha Gulf, White Sea

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Abstract

Chitin is among the most widespread biopolymers on Earth and occurs in high quantities in the exoskeletons of marine invertebrates. Chitinolytic bacteria are therefore typical components of marine ecosystems and play an important part in chitin biodegradation. The Kandalaksha Gulf area near the White Sea Biological Station, Moscow State University, which is inhabited by numerous invertebrates, is a promising site for the isolation of such bacteria. The composition of environmental prokaryotic communities and of enrichment cultures grown on chitin was determined, and pure cultures of active chitinolytics were isolated and identified as Pseudoalteromonas undina and Vibrio alginolyticus. The chitinolytic potential of the genera predominant in enrichment cultures was assessed; these may include previously unknown chitinolytic microorganisms.

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About the authors

A. M. Dukat

Moscow State University

Email: nycterix@mail.ru
Russian Federation, Moscow

A. M. Kuznetsova

Moscow State University

Author for correspondence.
Email: nycterix@mail.ru
Russian Federation, Moscow

S. D. Klyagin

Moscow State University

Email: nycterix@mail.ru
Russian Federation, Moscow

V. O. Trushin

Moscow State University

Email: nycterix@mail.ru
Russian Federation, Moscow

A. A. Klyukina

Winogradsky Institute of Microbiology, FRC Fundamentals of Biotechnology, Russian Academy of Sciences

Email: nycterix@mail.ru
Russian Federation, Moscow

A. G. Elcheninov

Winogradsky Institute of Microbiology, FRC Fundamentals of Biotechnology, Russian Academy of Sciences

Email: nycterix@mail.ru
Russian Federation, Moscow

I. V. Danilova

Moscow State University

Email: nycterix@mail.ru
Russian Federation, Moscow

References

  1. Варламов В. П., Ильина А. В., Шагдарова Б. Ц., Луньков А. П., Мысякина И. С. Хитин/хитозан и его производные: фундаментальные и прикладные аспекты // Успехи биологической химии. 2020. Т. 60. С. 317‒368.
  2. Varlamov V. P., Il’ina A.V., Shagdarova B. Ts., Lunkov A. P., Mysyakina I. S. Chitin/chitosan and its derivatives: fundamental problems and practical approaches // Biochemistry (Moscow). 2020. V. 85. Suppl. 1. P. S154‒S176. https://doi.org/10.1134/S0006297920140084
  3. Azizi A., Mohd Hanafi N., Basiran M. N., Teo C. H. Evaluation of disease resistance and tolerance to elevated temperature stress of the selected tissue-cultured Kappaphycus alvarezii Doty 1985 under optimized laboratory conditions // 3 Biotech. 2018. V. 8. P. 321. https://doi.org/10.1007/s13205-018-1354-4
  4. Barbieri E., Falzano L., Fiorentini C., Pianetti A., Baffone W., Fabbri A., Matarrese P., Casiere A., Katouli M., Kühn I., Möllby R., Bruscolini F., Donelli G. Occurrence, diversity, and pathogenicity of halophilic Vibrio spp. and non-O1 Vibrio cholerae from estuarine waters along the Italian Adriatic coast // Appl. Environ. Microbiol. 1999. V. 65. P. 2748‒2753.
  5. Berlemont R., Martiny A. C. Genomic potential for polysaccharide deconstruction in bacteria //Appl. Environ. Microbiol. 2015. V. 81. P. 1516‒1517.
  6. Boliang G., Min J., Li L., Wu Q., Runying Z. Genome sequencing reveals the complex polysaccharide-degrading ability of novel deep-sea bacterium Flammeovirga pacifica WPAGA1 // Front. Microbiol. 2017. V. 8. P. 6–9.
  7. 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 QIIME2 // Nat. Biotechnol. 2019. V. 37. P. 852–857.
  8. Chan K., Baumann L., Garza M., Baumann P. Two new species of Alteromonas: Alteromonas espejiana and Alteromonas undina // Int. J. Syst. Bacteriol. 1978. V. 28. P. 217–222.
  9. Cho H. A. Isolation and characterization of alginate-degrading Pseudoalteromonas sp. Y-4: diss. — 부경대학교, 2011. P. 34‒48.
  10. Drula E., Garron M. L., Dogan S., Lombard V., Henrissat B., Terrapon N. The carbohydrate-active enzyme database: functions and literature // Nucl. Acids Res. 2022. V. 50 (D1). P. D571‒D577.
  11. Foster A. B., Webber J. M. Chitin // Adv. Carbohydr. Chem. 1961. V. 15. P. 371‒393.
  12. 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. V. 10. Art. 1573.
  13. https://doi.org/10.3389/fmicb.2019.01573
  14. González J. M., Mayer F., Moran M. A., Hodson R. E., Whitman W. B. Microbulbifer hydrolyticus gen. nov., sp. nov., and Marinobacterium georgiense gen. nov., sp. nov., two marine bacteria from a lignin-rich pulp mill waste enrichment community // Int. J. Syst. Bacteriol. 1997. V. 47. P. 369–376.
  15. Hackbusch S., Wichels A., Gimenez L., Döpke H., Gerdts G. Potentially human pathogenic Vibrio spp. in a coastal transect: occurrence and multiple virulence factors // Sci. Total Environ. 2020. V. 707. P. 113–136.
  16. Han F., Zhang M., Shang H., Liu Z., Zhou W. Microbial community succession, species interactions and metabolic pathways of sulfur-based autotrophic denitrification system in organic-limited nitrate wastewater // Bioresour. Technol. 2020. V. 315. Art. 123826. https://doi.org/10.1016/j.biortech.2020.123826
  17. Huq A., West P. A., Smal E. B., Huq M. I., Colwell R. R. Influence of water temperature, salinity, and pH on survival and growth of toxigenic Vibrio cholerae serovar 01 associated with live copepods in laboratory microcosms // Appl. Environ. Microbiol. 1984. V. 48. P. 420‒424.
  18. Imran M., Ghadi S. C. Role of carbohydrate active enzymes (CAZymes) in production of marine bioactive oligosaccharides and their pharmacological applications // Enzymatic technologies for marine polysaccharides / Ed. A. Trincone. Boca Raton: CRC Press, 2019. P. 357‒374.
  19. Imran M., Poduval P. B., Ghadi S. C. Bacterial degradation of algal polysaccharides in marine ecosystem // Marine pollution and microbial remediation / Eds. M. Naik, S. Dubey. Singapore: Springer, 2017. P. 189‒203.
  20. Isipato M., Dessì P., Sánchez C., Mills S., Ijaz U. Z., Asunis F., Spiga D., De Gioannis G., Mascia M., Collins G., Muntoni A., Lens P. N.L. Propionate production by bioelectrochemicaly-assisted lactate fermentation and simultaneous CO2 recycling // Front. Microbiol. 2020. V. 11. Art. 599438. https://doi.org/10.3389/fmicb.2020.599438
  21. Ohishi K., Yamagishi M., Ohta T., Suzuki M., Izumida H., Sano H., Nishijima M., Miwa T. Purification and properties of two chitinases from Vibrio alginolyticus H-8 // J. Ferment. Bioengin. 1996. V. 82. P. 598‒600.
  22. Kelbrick M., Abed R. M.M., Antunes A. Motilimonas cestriensis sp. nov., isolated from an inland brine spring in Northern England // Int. J. Syst. Evol. Microbiol. 2019. V. 71. Art. 004763. https://doi.org/10.1099/ijsem.0.004763
  23. Liu G., Wu S., Jin W., Sun C. Amy63, a novel type of marine bacterial multifunctional enzyme possessing amylase, agarase and carrageenase activities // Sci. Rep. 2016. V. 6. Art. 18726. P. 1–12.
  24. https://doi.org/10.1038/srep18726
  25. Lobo S. A., Warren M. J., Saraiva L. M. Sulfate-reducing bacteria reveal a new branch of tetrapyrrole metabolism // Adv. Microb. Physiol. 2012. V. 61. P. 267‒295.
  26. Ma C., Lu X., Shi C., Li J., Gu Y., Ma Y., Chu Y., Han F., Gong Q., Yu W. Molecular cloning and characterization of a novel β-agarase, AgaB, from marine Pseudoalteromonas sp. CY24 // J. Biol. Chem. 2007. V. 282. P. 3747‒3754.
  27. Malecki P. H., Raczynska J. E., Vorgias C. E., Rypniewski W. Structure of a complete four-domain chitinase from Moritella marina, a marine psychrophilic bacterium // Acta Crystalogr. D Biol. Crystalogr. 2013. V. 69. P. 821‒829.
  28. Mancuso M., Costanzo M. T., Maricchiolo G., Gristina M., Zaccone R., Cuccu D., Genovese L. Characterization of chitinolytic bacteria and histological aspects of Shell Disease Syndrome in European spiny lobsters (Palinurus elephas) (Fabricius 1787) // J. Invertebr. Pathol. 2010. V. 104. P. 242‒244.
  29. Masselin A., Rousseau A., Pradeau S., Fort L., Gueret R., Buon L., Armand S., Cottaz S., Choisnard L., Fort S. Optimizing chitin depolymerization by lysozyme to long-chain oligosaccharides // Mar. Drugs. 2021. V. 19. Art. 320. https://doi.org/10.3390/md19060320
  30. Matsumoto A., Kawai S. J., Yamada M. Utilization of various carbon sources for poly(3-hydroxybutyrate) [P(3HB)] production by Cobetia sp. IU180733JP01 (5–11–6–3) which is capable of producing P(3HB) from alginate and waste seaweed // J. Gen. Appl. Microbiol. 2022. V. 68. P. 207‒211.
  31. Médigue C., Krin E., Pascal G., Barbe V., Bernsel A., Bertin P. N., Cheung F., Cruveiller S., D’Amico S., Duilio A., Fang G., Feller G., Ho C., Mangenot S., Marino G., Nilsson J., Parrilli E., Rocha E. P., Rouy Z., Sekowska A., Tutino M. L., Vallenet D., von Heijne G., Danchin A. Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125 // Genome Res. 2005. V. 15. P. 1325–1335.
  32. Mouchka M. E., Hewson I., Harvell C. D. Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts // Integr. Comp. Biol. 2010. V. 50. P. 662‒674.
  33. Muñoz G., Zuluaga F. Biological activities and application of marine polysaccharides / Ed. E. A. Shalaby. InTech, 2017. 328 p. Ch. 5. P. 87‒106. https://doi.org/10.5772/66527
  34. Neave M. J., Apprill A., Ferrier-Pagès C., Voolstra C. R. Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas // Appl. Microbiol. Biotechnol. 2016. V. 100. P. 8315‒8324.
  35. Nygren A., Parapar J., Pons J., Meißner K., Bakken T., Kongsrud J. A., Oug E., Gaeva D., Sikorski A., Johansen R. A., Hutchings P. A., Lavesque N., Capa M. A mega-cryptic species complex hidden among one of the most common annelids in the North East Atlantic // PLoS One. 2018. V. 13. e0198356. https://doi.org/10.1371/journal.pone.0198356
  36. Paulsen S. S., Andersen B., Gram L., Machado H. Biological potential of chitinolytic marine bacteria // Mar. Drugs. 2016. V. 14. Art. 230. https://doi.org/10.3390/md14120230
  37. Paulsen S. S., Strube M. L., Bech P. K., Gram L., Sonnenschein E. C. Marine chitinolytic Pseudoalteromonas represents an untapped reservoir of bioactive potential // mSystems. 2019. V. 4. e00060–19. https://doi.org/10.1128/mSystems.00060-19
  38. Pesciaroli C., Cupini F., Selbmann L., Barghini P., Fenice M. Temperature preferences of bacteria isolated from seawater collected in Kandalaksha Bay, White Sea, Russia // Polar Biol. 2012. V. 35. P. 435–445.
  39. Pike R. E., Haltli B., Kerr R. G. Description of Endozoicomonas euniceicola sp. nov. and Endozoicomonas gorgoniicola sp. nov., bacteria isolated from the octocorals Eunicea fusca and Plexaura sp., and an emended description of the genus Endozoicomonas // Int. J. Syst. Evol. Microbiol. 2013. V. 63. P. 4294‒4302.
  40. Ringø E., Hoseinifar S. H., Ghosh K., Doan H. V., Beck B. R., Song S. K. Lactic acid bacteria in finfish-an update // Front. Microbiol. 2018. V. 9. Art. 1818. https://doi.org/10.3389/fmicb.2018.01818
  41. Seki H. Microbiological studies on the decomposition of chitin in marine environment-IX // J. Oceanogr. Soc. Japan. 1965. V. 21. № 6. P. 253‒260.
  42. Skåne A., Minniti G., Loose J. S.M., Mekasha S., Bissaro B., Mathiesen G., Arntzen M. Ø., Vaaje-Kolstad G. The fish pathogen Aliivibrio salmonicida LFI1238 can degrade and metabolize chitin despite gene disruption in the chitinolytic pathway // Appl. Environ. Microbiol. 2021. V. 87. e0052921. https://doi.org/10.1128/AEM.00529-21
  43. 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.
  44. Sorokin D. Y., Kuenen J. G. Chemolithotrophic haloalkaliphiles from soda lakes // FEMS Microbiol Ecol. 2005. V. 52. P. 287‒295.
  45. Tarsi R., Pruzzo C. Role of surface proteins in Vibrio cholerae attachment to chitin // Appl. Environ. Microbiol. 1999. V. 65. P. 1348–1351.
  46. Teramoto M., Suzuki M., Okazaki F., Hatmanti A., Harayama S. Oceanobacter-related bacteria are important for the degradation of petroleum aliphatic hydrocarbons in the tropical marine environment // Microbiology (SGM). 2009. V. 155. P. 3362‒3370.
  47. Tomco P. L., Duddleston K. N., Driskill A., Hatton J. J., Grond K., Wrenn T., Tarr M. A., Podgorski D. C., Zito P. Dissolved organic matter production from herder application and in-situ burning of crude oil at high latitudes: Bioavailable molecular composition patterns and microbial community diversity effects // J. Hazard Mater. 2022. V. 424. Pt. C. Art. 127598. https://doi.org/10.1016/j.jhazmat.2021.127598
  48. Vortsepneva E., Chevaldonné P., Klyukina A., Naduvaeva E., Todt C., Zhadan A., Tzetlin A., Kublanov I. Microbial associations of shalow-water mediterranean marine cave Solenogastres (Mollusca) // PeerJ. 2021. V. 9. P. e12655. https://doi.org/10.7717/peerj.12655
  49. Wang X., Zhao Y., Tan H., Chi N., Zhang Q., Du Y., Yin H. Characterisation of a chitinase from Pseudoalteromonas sp. DL-6, a marine psychrophilic bacterium // Int. J. Biol. Macromol. 2014. V. 70. P. 455‒462.
  50. Wang X., Isbrandt T., Strube M. L., Paulsen S. S., Nielsen M. W., Buijs Y., Schoof E. M., Larsen T. O., Gram L., Zhang S. D. Chitin degradation machinery and secondary metabolite profiles in the marine bacterium Pseudoalteromonas rubra S4059 // Mar. Drugs. 2021. V. 19. Art. 108. https://doi.org/10.3390/md19020108
  51. Wang X., Li Y., Xue C. X., Li B., Zhou S., Liu L., Zhang X. H. Photobacterium chitinilyticum sp. nov., a marine bacterium isolated from seawater at the bottom of the East China Sea // Int. J. Syst. Evol. Microbiol. 2019. V. 69. P. 1477‒1483.
  52. Wenzel M. A., Douglas A., Piertney S. B. Microbiome composition within a sympatric species complex of intertidal isopods (Jaera albifrons) // PLoS One. 2018. V. 13. Art. 0202212.
  53. https://doi.org/10.1371/journal.pone.0202212
  54. Zheng J., Ge Q., Yan Y., Zhang X., Huang L., Yin Y. dbCAN3: automated carbohydrate-active enzyme and substrate annotation // Nucl. Acids Res. 2023. V. 51. P. W115–W121. https://doi.org/10.1093/nar/gkad328
  55. Zheng Q., Meng X., Cheng M., Li Y., Liu Y., Chen X. Cloning and characterization of a new chitosanase from a deep-sea bacterium Serratia sp. QD07 // Front. Microbiol. 2021. V. 12. Art. 619731. https://doi.org/10.3389/fmicb.2021.619731
  56. Zobell C. E., Rittenberg S. C. The occurrence and characteristics of chitinoclastic bacteria in the sea // J. Bacteriol. 1938. V. 35. P. 275‒287.
  57. Zou Y., Robbens J., Heyndrickx M., Debode J., Raes K. quantification of extracellular proteases and chitinases from marine bacteria // Curr. Microbiol. 2020. V. 77. P. 3927‒3936.

Supplementary files

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2. Fig. 1. Composition of the microbial community associated with Copepoda sp. CN (a) and the resulting CE storage culture utilizing chitin as the sole source of carbon and energy (b)

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3. Fig. 2. Composition of the microbial community associated with Terebillides sp. TN (a) and the resulting accumulative TE culture utilizing chitin as the sole source of carbon and energy (b)

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4. Fig. 3. Composition of the microbial community of an accumulation culture of ME obtained from a water sample of the Kandalaksha Bay and utilizing chitin as the only source of carbon and energy

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5. Fig. 4. Chitin hydrolysis zones on Petri dishes with pure cultures of Pseudoalteromonas undina P1 (a) and Vibrio alginolyticus C1 (b)

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6. Fig. 5. Sets of putative chitinases and peptidoglycan-hydrolyzing enzymes encoded in the genomes of Cobetia and Endozoicomonas representatives

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