Skip to main content
Log in

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

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Chitin is one of 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 biodegradation. The Kandalaksha Bay 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 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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

REFERENCES

  1. Azizi, A., Mohd Hanafi, N., Basiran, M.N., and 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, vol. 8, p. 321. https://doi.org/10.1007/s13205-018-1354-4

  2. Barbieri, E., Falzano, L., Fiorentini, C., Pianetti, A., Baffone, W., Fabbri, A., Matarrese, P., Casiere, A., Katouli, M., Kühn, I., Möllby, R., Bruscolini, F., and 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, vol. 65, pp. 2748‒2753.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Berlemont, R. and Martiny, A.C., Genomic potential for polysaccharide deconstruction in bacteria, Appl. Environ. Microbiol., 2015, vol. 81, pp. 1516‒1517.

    Article  Google Scholar 

  4. Boliang, G., Min, J., Li, L., Wu, Q., and Runying, Z., Genome sequencing reveals the complex polysaccharide-degrading ability of novel deep-sea bacterium Flammeovirga pacifica WPAGA1, Front. Microbiol., 2017, vol. 8, pp. 6–9.

    Google Scholar 

  5. 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., Bai, Y., Bisanz, J.E., Bittinger, K., Brejnrod A., Brislawn, C.J., et al., Two new species of Alteromonas: Alteromonas espejiana and Alteromonas undina, Int. J. Syst. Bacteriol., 1978, vol. 28, pp. 217–222.

    Article  Google Scholar 

  6. Cho, H.A., Isolation and characterization of alginate-degrading Pseudoalteromonas sp. Y-4, Dissertation, Bugyung University, 2011, pp. 34‒48.

  7. Drula, E., Garron, M.L., Dogan, S., Lombard, V., Henrissat, B., and Terrapon, N., The carbohydrate-active enzyme database: functions and literature, Nucl. Acids Res., 2022, vol. 50 (D1), pp. D571‒D577.

    Article  CAS  PubMed  Google Scholar 

  8. Foster, A.B. and Webber, J.M., Chitin, Adv. Carbohydr. Chem., 1961, vol. 15, pp. 371‒393.

    CAS  Google Scholar 

  9. Gavrilov, S.N., Korzhenkov, A.A., Kublanov, I.V., Bargiela, R., Zamana, L.V., Popova, A.A., Peter, S.V., Golyshin, N., and Golyshina, O.V., Microbial communities of polymetallic deposits’ acidic ecosystems of continental climatic zone with high temperature contrasts, Front. Microbiol., 2019, vol. 10, p. 1573. https://doi.org/10.3389/fmicb.2019.01573

    Article  PubMed  PubMed Central  Google Scholar 

  10. González, J.M., Mayer, F., Moran, M.A., Hodson, R.E., and 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, vol. 47, pp. 369–376.

    Article  PubMed  Google Scholar 

  11. Hackbusch, S., Wichels, A., Gimenez, L., Döpke, H., and Gerdts, G., Potentially human pathogenic Vibrio spp. in a coastal transect: occurrence and multiple virulence factors, Sci. Total Environ., 2020, vol. 707, pp. 113–136.

    Article  Google Scholar 

  12. Han, F., Zhang, M., Shang, H., Liu, Z., and Zhou, W., Microbial community succession, species interactions and metabolic pathways of sulfur-based autotrophic denitrification system in organic-limited nitrate wastewater, Bioresour. Technol., 2020, vol. 315, p. 123826. https://doi.org/10.1016/j.biortech.2020.123826

    Article  CAS  PubMed  Google Scholar 

  13. Huq, A., West, P.A., Smal, E.B., Huq, M.I., and 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, vol. 48, pp. 420‒424.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Imran, M. and Ghadi, S.C., Role of carbohydrate active enzymes (CAZymes) in production of marine bioactive oligosaccharides and their pharmacological applications, in Enzymatic Technologies for Marine Polysaccharides, Trincone, A., Ed., Boca Raton: CRC Press, 2019, pp. 357‒374.

    Google Scholar 

  15. Imran, M., Poduval, P.B., and Ghadi, S.C., Bacterial degradation of algal polysaccharides in marine ecosystem, in Marine Pollution and Microbial Remediation, Naik, M. and Dubey, S., Eds., Singapore: Springer, 2017, pp. 189‒203.

    Google Scholar 

  16. Isipato, M., Dessì, P., Sánchez, C., Mills, S., Ijaz, U.Z., Asunis, F., Spiga, D., De Gioannis, G., Mascia, M., Collins, G., Muntoni, A., and Lens, P.N.L., Propionate production by bioelectrochemicaly-assisted lactate fermentation and simultaneous CO2 recycling, Front. Microbiol., 2020, vol. 11, p. 599438. https://doi.org/10.3389/fmicb.2020.599438

    Article  PubMed  PubMed Central  Google Scholar 

  17. Kelbrick, M., Abed, R.M.M., and Antunes, A., Motilimonas cestriensis sp. nov., isolated from an inland brine spring in Northern England, Int. J. Syst. Evol. Microbiol., 2019, vol. 71, p. 004763. https://doi.org/10.1099/ijsem.0.004763

    Article  CAS  PubMed  Google Scholar 

  18. Liu, G., Wu, S., Jin, W., and Sun, C., Amy63, a novel type of marine bacterial multifunctional enzyme possessing amylase, agarase and carrageenase activities, Sci. Rep., 2016, vol. 6, art. 18726, pp. 1–12. https://doi.org/10.1038/srep18726

  19. Lobo, S.A., Warren, M.J., and Saraiva, L.M., Sulfate-reducing bacteria reveal a new branch of tetrapyrrole metabolism, Adv. Microb. Physiol., 2012, vol. 61, pp. 267‒295.

    Article  CAS  PubMed  Google Scholar 

  20. Ma, C., Lu, X., Shi, C., Li, J., Gu, Y., Ma, Y., Chu, Y., Han, F., Gong, Q., and Yu, W., Molecular cloning and characterization of a novel β-agarase, AgaB, from marine Pseudoalteromonas sp. CY24, J. Biol. Chem., 2007, vol. 282, pp. 3747‒3754.

    Article  CAS  PubMed  Google Scholar 

  21. Malecki, P.H., Raczynska, J.E., Vorgias, C.E., and Rypniewski, W., Structure of a complete four-domain chitinase from Moritella marina, a marine psychrophilic bacterium, Acta Crystalogr. D Biol. Crystalogr., 2013, vol. 69, pp. 821‒829.

    Article  CAS  Google Scholar 

  22. Mancuso, M., Costanzo, M.T., Maricchiolo, G., Gristina, M., Zaccone, R., Cuccu, D., and 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, vol. 104, pp. 242‒244.

    Article  CAS  PubMed  Google Scholar 

  23. Masselin, A., Rousseau, A., Pradeau, S., Fort, L., Gueret, R., Buon, L., Armand, S., Cottaz, S., Choisnard, L., and Fort, S., Optimizing chitin depolymerization by lysozyme to long-chain oligosaccharides, Mar. Drugs, 2021, vol. 19, p. 320. https://doi.org/10.3390/md19060320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Matsumoto, A., Kawai, S.J., and 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, vol. 68, pp. 207‒211.

    Article  CAS  PubMed  Google Scholar 

  25. 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., et al., Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125, Genome Res., 2005, vol. 15, pp. 1325–1335.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Mouchka, M.E., Hewson, I., and Harvell, C.D., Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts, Integr. Comp. Biol., 2010, vol. 50, pp. 662‒674.

    Article  PubMed  Google Scholar 

  27. Muñoz, G. and Zuluaga, F., Biological Activities and Application of Marine Polysaccharides, Shalaby, E.A., Ed., InTech, 2017, ch. 5, pp. 87‒106. https://doi.org/10.5772/66527

    Book  Google Scholar 

  28. Neave, M.J., Apprill, A., Ferrier-Pagès, C., and Voolstra, C.R., Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas, Appl. Microbiol. Biotechnol., 2016, vol. 100, pp. 8315‒8324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 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., and Capa, M., A mega-cryptic species complex hidden among one of the most common annelids in the North East Atlantic, PLoS One, 2018, vol. 13, p. e0198356. https://doi.org/10.1371/journal.pone.0198356

    Article  CAS  Google Scholar 

  30. Ohishi, K., Yamagishi, M., Ohta, T., Suzuki, M., Izumida, H., Sano, H., Nishijima, M., and Miwa, T., Purification and properties of two chitinases from Vibrio alginolyticus H-8, J. Ferment. Bioengin., 1996, vol. 82, pp. 598‒600.

    Article  CAS  Google Scholar 

  31. Paulsen, S.S., Andersen, B., Gram, L., and Machado, H., Biological potential of chitinolytic marine bacteria, Mar. Drugs, 2016, vol. 14, p. 230. https://doi.org/10.3390/md14120230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Paulsen, S.S., Strube, M.L., Bech, P.K., Gram, L., and Sonnenschein, E.C., Marine chitinolytic Pseudoalteromonas represents an untapped reservoir of bioactive potential, mSystems, 2019, vol. 4, p. e00060-19. https://doi.org/10.1128/mSystems.00060-19

    Article  Google Scholar 

  33. Pesciaroli, C., Cupini, F., Selbmann, L., Barghini, P., and Fenice, M., Temperature preferences of bacteria isolated from seawater collected in Kandalaksha Bay, White Sea, Russia, Polar Biol., 2012, vol. 35, pp. 435–445.

    Article  Google Scholar 

  34. Pike, R.E., Haltli, B., and 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, vol. 63, pp. 4294‒4302.

    Article  CAS  PubMed  Google Scholar 

  35. Ringø, E., Hoseinifar, S.H., Ghosh, K., Doan, H.V., Beck, B.R., and Song, S.K. Lactic acid bacteria in finfish‒an update, Front. Microbiol., 2018, vol. 9, p. 1818. https://doi.org/10.3389/fmicb.2018.01818

    Article  PubMed  PubMed Central  Google Scholar 

  36. Seki, H., Microbiological studies on the decomposition of chitin in marine environment-IX, J. Oceanogr. Soc. Japan, 1965, vol. 21, no. 6, pp. 253‒260.

    Article  Google Scholar 

  37. Skåne, A., Minniti, G., Loose, J.S.M., Mekasha, S., Bissaro, B., Mathiesen, G., Arntzen, M.Ø., and 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, vol. 87, p. e0052921. https://doi.org/10.1128/AEM.00529-21

    Article  Google Scholar 

  38. 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, vol. 5, pp. 1‒34.

    Google Scholar 

  39. Sorokin, D.Y. and Kuenen, J.G., Chemolithotrophic haloalkaliphiles from soda lakes, FEMS Microbiol Ecol., 2005, vol. 52, pp. 287‒295.

    Article  CAS  PubMed  Google Scholar 

  40. Tarsi, R. and Pruzzo, C., Role of surface proteins in Vibrio cholerae attachment to chitin, Appl. Environ. Microbiol., 1999, vol. 65, pp. 1348–1351.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Teramoto, M., Suzuki, M., Okazaki, F., Hatmanti, A., and Harayama, S., Oceanobacter-related bacteria are important for the degradation of petroleum aliphatic hydrocarbons in the tropical marine environment, Microbiology (SGM), 2009, vol. 155, pp. 3362‒3370.

    Article  CAS  PubMed  Google Scholar 

  42. Tomco, P.L., Duddleston, K.N., Driskill, A., Hatton, J.J., Grond, K., Wrenn, T., Tarr, M.A., Podgorski, D.C., and 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, vol. 424, part. C, p. 127598. https://doi.org/10.1016/j.jhazmat.2021.127598

    Article  CAS  PubMed  Google Scholar 

  43. Varlamov, V.P., Il’ina, A.V., Shagdarova, B.Ts., Lunkov, A.P., and Mysyakina, I.S., Chitin/chitosan and its derivatives: fundamental problems and practical approaches, Biochemistry (Moscow), 2020, vol. 85, Suppl. 1, pp. S154‒S176. https://doi.org/10.1134/S0006297920140084

    Article  CAS  PubMed  Google Scholar 

  44. Vortsepneva, E., Chevaldonné, P., Klyukina, A., Naduvaeva, E., Todt, C., Zhadan, A., Tzetlin, A., and Kublanov, I., Microbial associations of shalow-water mediterranean marine cave Solenogastres (Mollusca), PeerJ., 2021, vol. 9, p. e12655. https://doi.org/10.7717/peerj.12655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Wang, X., Isbrandt, T., Strube, M.L., Paulsen, S.S., Nielsen, M.W., Buijs, Y., Schoof, E.M., Larsen, T.O., Gram, L., and Zhang, S.D., Chitin degradation machinery and secondary metabolite profiles in the marine bacterium Pseudoalteromonas rubra S4059, Mar. Drugs, 2021, vol. 19, p. 108. https://doi.org/10.3390/md19020108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Wang, X., Li, Y., Xue, C.X., Li, B., Zhou, S., Liu, L., and 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, vol. 69, pp. 1477‒1483.

    Article  CAS  PubMed  Google Scholar 

  47. Wang, X., Zhao, Y., Tan, H., Chi, N., Zhang, Q., Du, Y., and Yin, H., Characterisation of a chitinase from Pseudoalteromonas sp. DL-6, a marine psychrophilic bacterium, Int. J. Biol. Macromol., 2014, vol. 70, pp. 455‒462.

    Article  CAS  PubMed  Google Scholar 

  48. Wenzel, M.A., Douglas, A., and Piertney, S.B., Microbiome composition within a sympatric species complex of intertidal isopods (Jaera albifrons), PLoS One, 2018, vol. 13, p. 0202212. https://doi.org/10.1371/journal.pone.0202212

    Article  CAS  Google Scholar 

  49. Zheng, J., Ge, Q., Yan, Y., Zhang, X., Huang, L., and Yin, Y., dbCAN3: automated carbohydrate-active enzyme and substrate annotation, Nucl. Acids Res., 2023, vol. 51, pp. W115–W121. https://doi.org/10.1093/nar/gkad328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zheng, Q., Meng, X., Cheng, M., Li, Y., Liu, Y., and Chen, X., Cloning and characterization of a new chitosanase from a deep-sea bacterium Serratia sp. QD07, Front. Microbiol., 2021, vol. 12, p. 619731. https://doi.org/10.3389/fmicb.2021.619731

    Article  PubMed  PubMed Central  Google Scholar 

  51. Zobell, C.E. and Rittenberg, S.C., The occurrence and characteristics of chitinoclastic bacteria in the sea, J. Bacteriol. 1938, vol. 35, pp. 275‒287.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Zou, Y., Robbens, J., Heyndrickx, M., Debode, J., and Raes, K., Quantification of extracellular proteases and chitinases from marine bacteria, Curr. Microbiol., 2020, vol. 77, pp. 3927‒3936.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The work was supported by the Ministry of Science and Higher Education of the Russian Federation, Agreement 075-15-2021-1396.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. M. Kuznetsova.

Ethics declarations

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Translated by P. Sigalevich

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dukat, A.M., Kuznetsova, A.M., Klyagin, S.D. et al. Chitin Degradation by Microbial Communities of the Kandalaksha Bay, White Sea. Microbiology 93, 61–78 (2024). https://doi.org/10.1134/S0026261723603111

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261723603111

Keywords:

Navigation