Structural diversity and properties of carbohydrate containing biopolymers of marine Gram-negative bacteria

Cover Page

Cite item

Full Text

Abstract

Results of the studies of the capsular polysaccharides and lipopolysaccharides from the marine Gram-negative bacteria belonging to the genera Pseudoalteromonas, Idiomarina, Marinicella, Halomonas, Cobetia, Poseidonocella, Psychrobacter, Devosia, Echinicola and Cellulophaga are presented.

Full Text

Restricted Access

About the authors

Maxim S. Kokoulin

G.B. Elyakov Pacific Institute of Bioorganic Chemistry, FEB RAS

Author for correspondence.
Email: maxchem@mail.ru
ORCID iD: 0000-0003-2245-6802

Candidate of Sciences in Chemistry, Senior Researcher

Russian Federation, Vladivostok

Alexandra S. Kuzmich

G.B. Elyakov Pacific Institute of Bioorganic Chemistry, FEB RAS

Email: assavina@mail.ru
ORCID iD: 0000-0001-5358-5880

Researcher

Russian Federation, Vladivostok

Alina P. Filshtein

G.B. Elyakov Pacific Institute of Bioorganic Chemistry, FEB RAS

Email: alishichka@mail.ru
ORCID iD: 0009-0000-6293-6582

Candidate of Sciences in Chemistry, Junior Researcher

Russian Federation, Vladivostok

References

  1. Rothschild L. J., Mancinelli R. L. Life in extreme environments. Nature. 2001;409(6823):1092-1100.
  2. Di Lorenzo F., Duda K. A., Lanzetta R., Silipo A., De Castro C., Molinaro A. A. Journey from structure to function of bacterial lipopolysaccharides. Chem. Rev. 2022;122(20):15767-15821.
  3. Poli A., Anzelmo G., Nicolaus B. Bacterial exopolysaccharides from extreme marine habitats: Production, characterization and biological activities. Mar. Drugs. 2010;8:1779-1802.
  4. Casillo A., Lanzetta R., Parrilli M., Corsaro M. M. Exopolysaccharides from marine and marine extremophilic bacteria: Structures, properties, ecological roles and applications. Mar. Drugs. 2018;16:69.
  5. Nazarenko E. L., Komandrova N. A., Gorshkova R. P., Tomshich S. V., Zubkov V. A., Kilcoyne M., Savage A. V. Structures of polysaccharides and oligosaccharides of some Gram-negative marine Proteobacteria. Carbohydr. Res. 2003;338:2449-2457.
  6. Leone S., Silipo A., Nazarenko E. L., Lanzetta R., Parrilli M., Molinaro A. Molecular structure of endotoxins from Gram-negative marine bacteria: an update. (Review). Mar. Drugs. 2007;5(3):85-112.
  7. Nazarenko E. L., Crawford R. J., Ivanova E. P. The structural diversity of carbohydrate antigens of selected gram-negative marine bacteria. Mar. Drugs. 2011;9(10):1914-1954.
  8. Di Lorenzo F., Billod J.-M., Martin-Santamaria S., Silipo A., Molinaro A. Gram-negative extremophile lipopolysaccharides: Promising source of inspiration for a new generation of endotoxin antagonists. European. J. Org. Chem. 2017;28:4055-4073.
  9. Garcia-Vello P., Di Lorenzo F., Zucchetta D., Zamyatina A., De Castro C., Molinaro A. Lipopolysaccharide lipid A: A promising molecule for new immunity-based therapies and antibiotics. Pharmacol. Ther. 2022;230. 107970.
  10. Molinaro A., Holst O., Di Lorenzo F., Callaghan M., Nurisso A., D’Errico G., Zamyatina A., Peri F., Berisio R., Jerala R., Jiménez-Barbero J., Silipo A., Martín-Santamaría S. Chemistry of lipid A: at the heart of innate immunity. Chemistry. 2015;21:500-519.
  11. Romanenko L. A., Zhukova N. V., Rhode M., Lysenko A. M., Mikhailov V. V., Stackebrandt E. Pseudoalteromonas agarivorans sp. nov., a novel marine agarolytic bacterium. Int. J. Syst. Evol. Microbiol. 2003;53:125-131.
  12. Komandrova N. A., Tomshich S. V., Isakov V. V., Romanenko L. A. Structure of sulfated O-specific polysaccharide of the marine bacterium Pseudoalteromonas marinoglutinosa KMM 232. Dadianji Jishu. 1998;6:1410-1415.
  13. Kokoulin M. S., Komandrova N. A., Kalinovskiy A., Tomshich S. V., Romanenko L. A., Vaskovsky V. E. Structure of the O-specific polysaccharide from the deep-sea marine bacterium Idiomarina abyssalis KMM 227T containing a 2-O-sulfate-3-N-(4-hydroxybutanoyl)-3,6-dideoxy-D-glucose. Carbohydr. Res. 2015;413:100-106.
  14. Kokoulin M. S., Lizanov I. N., Romanenko L. A.., Chikalovets I. V. Structure of phosphorylated and sulfated polysaccharides from lipopolysaccharide of marine bacterium Marinicella litoralis KMM 3900T. Carbohydr. Res. 2020;490. 107961.
  15. Kokoulin M. S., Filshtein A. P., Romanenko, L.A., Chikalovets I. V., Chernikov O. V. Structure and bioactivity of sulfated α-D-mannan from marine bacterium Halomonas halocynthiae KMM 1376T. Carbohydr. Polym. 2020;229. 115556.
  16. Knirel Y. A., Kochetkov N. K. The structure of lipopolysaccharides of gram-negative bacteria. III. The structure of O-antigens: A review. Biochemistry (Moscow). 1994;59(12):1325-1383.
  17. Peréz Recalde M., Noseda M. D., Pujol C. A., Carlucci M. J., Matulewicz M. C. Sulfated mannans from the red seaweed Nemalion helminthoides of the South Atlantic. Phytochemistry. 2009;70:1062-1068.
  18. Fernándeza P. V., Estevez J. M., Cerezo A. S., Ciancia M. Sulfated β-D-mannan from green seaweed Codium vermilara. Carbohydr. Polym. 2012;87:916-919.
  19. Cobet A. B., Wirsen C. Jr., Jones G. E. The effect of nickel on a marine bacterium, Arthrobacter marinus sp. nov. J. Gen. Microbiol. 1970;62(2):159-169.
  20. Baumann L., Baumann P., Mandel M., Allen R. D. Taxonomy of aerobic marine eubacteria. J. Bacteriol. 1972;110(1):402-429.
  21. Baumann L., Bowditch R. D., Baumann P. Description of Deleya gen. nov. created to accommodate the marine species Alcaligenes aestus, A. pacificus, A. cupidus, A. venustus, and Pseudomonas marina. Int. J. Syst. Bacteriol. 1983;33:793-802.
  22. Dobson S. J., Franzmann P. D. Unification of the genera Deleya (Baumann et al. 1983), Halomonas (Vreeland et al. 1980), and Halovibrio (Fendrich 1988) and the species Paracoccus halodenitrificans (Robinson and Gibbons 1952) into a single genus, Halomonas, and placement of the genus Zymobacter in the family Halomonadaceae. Int. J. Syst. Bacteriol. 1996;46:550-558.
  23. Arahal D. R., Castillo A. M., Ludwig W., Schleifer K. H., Ventosa A. Proposal of Cobetia marina gen. nov., comb. nov., within the family Halomonadaceae, to include the species Halomonas marina. Syst Appl Microbiol. 2002;25(2):207-211.
  24. Kim M. S., Roh S. W., Bae J. W. Cobetia crustatorum sp. nov., a novel slightly halophilic bacterium isolated from traditional fermented seafood in Korea. Int. J. Syst. Evol. Microbiol. 2010;60(3):620-626.
  25. Kokoulin M. S., Kalinovsky A. I., Komandrova N. A., Tomshich S. V., Romanenko L. A., Vaskovsky V. E. The sulfated O-specific polysaccharide from the marine bacterium Cobetia pacifica KMM 3879T. Carbohydr. Res. 2014;387(1):4-9.
  26. Kokoulin M. S., Kalinovskiy A. I., Komandrova N. A., Tomshich S. V., Romanenko L. A., Vaskovsky V. E. The new sulfated O-specific polysaccharide from marine bacterium Cobetia pacifica KMM 3878, containing 3,4-O-[(S)-1-carboxyethylidene]-d-galactose and 2,3-O-disulfate-D-galactose. Carbohydr. Res. 2014;397(1):46-51.
  27. Kokoulin M. S., Kuzmich A. S., Kalinovsky A. I., Tomshich S. V., Romanenko L. A., Mikhailov V. V., Komandrova N. A. Structure and anticancer activity of sulfated O-polysaccharide from marine bacterium Cobetia litoralis KMM 3880T. Carbohydr. Polym. 2016;154:55-61.
  28. Matsuda M., Hasui M., Okutani K. Structural Analysis of a Sulfated Polysaccharide from a Marine Pseudomonas. Nippon Suisan Gakkaishi. 1993;59(3):535-538.
  29. Matsuda M., Yamori T., Naitoh M., Okutani K. Structural revision of sulfated polysaccharide B-1 isolated from a marine Pseudomonas species and its cytotoxic activity against human cancer cell lines. Mar. Biotechnol. 2003;5:13-19.
  30. Kokoulin M. S., Sigida E. N., Kuzmich A. S., Ibrahim I. M., Fedonenko Yu.P., Konnova S. A. Structure and antiproliferative activity of the polysaccharide from Halomonas aquamarina related to Cobetia pacifica. Carbohydr. Polym. 2022;298. 120125.
  31. Kokoulin M. S., Kuzmich A. S., Kalinovsky A. I., Rubtsov E. S., Romanenko L. A., Mikhailov V. V., Komandrova N. A. Structure and in vitro anticancer activity of sulfated O-polysaccharide from marine bacterium Poseidonocella pacifica KMM 9010T. Carbohydr. Polym. 2017;178:406-411.
  32. Kokoulin M. S., Kuzmich A. S., Romanenko L. A., Menchinskaya E. S., Mikhailov V. V., Komandrova N. A., Chernikov O. V. Sulfated O-polysaccharide with anticancer activity from the marine bacterium Poseidonocella sedimentorum KMM 9023T. Carbohydr. Polym. 2018;202:157-163.
  33. Shashkov A. S., Streshinskaya G. M., Tulskaya E. M., Senchenkova S. N., Baryshnikova L. M., Dmitrenok A. S., Ostash B. E., Fedorenko V. A. Antonie Van Leeuwenhoek. 2016;109:923-936.
  34. Gil-Serrano A.M., Rodríguez-Carvajal M.A., Tejero-Mateo P., Espartero J. L., Thomas-Oates J., Ruiz-Sainz J.E., Ia-Claveria Buend A. M. Structural determination of a 5-O-methyl-deaminated neuraminic acid (Kdn)-containing polysaccharide isolated from Sinorhizobium fredii. Biochem. J. 1998;334:585-594.
  35. Knirel Y. A., Kocharova N. A., Shashkov A. S., Kochetkov N. K., Mamontova V. A., Solovéva T. F. Structure of the capsular polysaccharide of Klebsiella ozaenae serotype K4 containing 3-deoxy-D-glycero-D-galacto-nonulosonic acid. Carbohydr. Res. 1989;188:145-155.
  36. Kokoulin M. S., Kuzmich A. S., Romanenko L. A., Chikalovets I. V. Sulfated capsular polysaccharide from the marine bacterium Kangiella japonica inhibits T-47D cells growth in vitro. Carbohydr. Polym. 2022;290. 119477.
  37. Young N. M., Kreisman L. S., Stupak J., MacLean L.L., Cobb B. A., Richards J. C. Structural characterization and MHCII-dependent immunological properties of the zwitterionic O-chain antigen of Morganella morganii. Glycobiology. 2011;21(10):1266-1276.
  38. Kilcoyne M., Perepelov A. V., Tomshich S. V., Komandrova N. A., Shashkov A. S., Romanenko L. A., Knirel Y. A., Savage A. V. Structure of the O-polysaccharide of Idiomarina zobellii KMM 231T containing two unusual amino sugars with the free amino group, 4-amino-4,6-dideoxy-D-glucose and 2-amino-2-deoxy-L-guluronic acid. Carbohydr. Res. 2004;339(3):477-482.
  39. Kuzmich A. S., Romanenko L. A., Kokoulin M. S. Cell-cycle arrest and mitochondria-dependent apoptosis induction in T-47D cells by the capsular polysaccharide from the marine bacterium Kangiella japonica KMM 3897. Carbohydr. Polyme. 2023;320. 121237.
  40. Cavicchioli R., Thomas T. Extremophiles. In: Lederberg J., Alexander M., Bloom B. R., Hopwood D., Hull R., Iglewski B. H., Laskin A. I., Oliver S. G., Schaechter M., Summers W. C. (eds). Encylopedia of microbiology, 2nd edn. San Diego: Academic Press Inc; 2000. P. 317-337.
  41. Feller G., Gerday C. Psychrophilic enzymes: hot topics in cold adaptation. Nat. Rev. Microbiol. 2003;1:200-208.
  42. Kokoulin M. S., Kuzmich A. S., Romanenko L. A., Chikalovets I. V., Chernikov O. V. Structure and in vitro bioactivity against cancer cells of the capsular polysaccharide from the marine bacterium Psychrobacter marincola. Mar. Drugs. 2020;18(5):268.
  43. Casillo A., Ricciardelli A., Parrilli E., Tutino M. L., Corsaro M. M. Cell-wall associated polysaccharide from the psychrotolerant bacterium Psychrobacter arcticus 273-4: isolation, purification and structural elucidation. Extremophiles. 2020;24:63-70.
  44. Kondakova A. N., Novototskaya-Vlasova K.A., Arbatsky N. P., Drutskaya M. S., Shcherbakova V. A., Shashkov A. S., Gilichinsky D. A., Nedospasov S. A., Knirel Y. A. Structure of the O-specific polysaccharide from the lipopolysaccharide of Psychrobacter cryohalolentis K5T containing a 2,3,4-triacetamido-2,3,4-trideoxy-L-arabinose moiety. J. Nat. Prod. 2012;75:2236-2240.
  45. Kokoulin M. S., Kuzmich A. S., Romanenko L. A., Chikalovets I. V. Structure and in vitro antiproliferative activity of the acidic capsular polysaccharide from the deep-sea bacterium Psychrobacter submarinus KMM 225Т. Carbohydr. Polym. 2021;262. 117941 (1–8).
  46. Kondakova A. N., Novototskaya-Vlasova K.A., Shashkov A. S., Drutskaya M. S., Senchenkova S. N., Shcherbakova V. A., Gilichinsky D. A., Nedospasov S. A., Knirel Y. A. Structure of an acidic polysaccharide isolated from Psychrobacter maritimus 3pS containing a bacillosamine derivative. Carbohydr. Res. 2012;359:7-10.
  47. Leone S., Izzo V., Silipo A., Sturiale L., Garozzo D., Lanzetta R., Parrilli M., Molinaro A., Di Donato A. A novel type of highly negatively charged lipooligosaccharide from Pseudomonas stutzeri OX1 possessing two 4,6-O-(1-carboxy)-ethylidene residues in the outer core region. European. J. Org. Chem. 2004;271:2691-2704.
  48. Perepelov A. V., Weintraub A., Liu B., Senchenkova S. N., Shashkov A. S., Feng L., Wang L., Widmalm G., Knirel Y. A. The O-polysaccharide of Escherichia coli O112ac has the same structure as that of Shigella dysenteriae type 2 but is devoid of O-acetylation: a revision of the S. dysenteriae type 2 O-polysaccharide structure. Carbohydr. Res. 2008;343:977-981.
  49. Adeyeye A., Jansson P.-E., Lindberg B. Structural studies of the Escherichia coli O-149 O-antigen polysaccharide. Carbohydr. Res. 1988;176:231-236.
  50. Kokoulin M. S., Romanenko L. A., Kuzmich A. S., Chernikov O. V. Structure of the cell-wall-associated polysaccharides from the deep-sea marine bacterium Devosia submarina KMM 9415T. Mar. Drugs. 2021;19:665.
  51. Gilbert M., Mandrell R. E., Parker C. T., Li J., Vinogradov E. Structural analysis of the capsular polysaccharide from Campylobacter jejuni RM1221. ChemBioChem. 2007;8:625-631.
  52. Perepelov A. V., Senchenkova S. N., Kalinchuk N. A., Shashkov ,A.S., Knirel, Yu. A. Structure of O-polysaccharide of Escherichia coli O95: a disaccharide repeating unit containing D-fucose and D-threo-pent-2-ulose (xululose). Russ. Chem. Bull. 2018;67:1931-1933.
  53. Gorshkova R. P., Isakov V. V., Kalmykova E. N., Ovodov Y. S. Structural studies of O-specific polysaccharide chains of the lipopolysaccharide from Yersinia enterocolitica serovar O:10. Carbohydr. Res. 1995;268(2):249-255.
  54. Sato N., Nakazawa F., Ito T., Hoshino T., Hoshino E. The structure of the antigenic polysaccharide produced by Eubacterium saburreum T15. Carbohydr. Res. 2003;338(9):923-930.
  55. Jorgensen B. B., Boetius A. Feast and famine – Microbial life in the deep-sea bed. Nat. Rev. Microbiol. 2007;5:770-781.
  56. Kallmeyer J., Pockalny R., Adhikari R. R., Smith D. C., D’Hondt S. Global distribution of microbial abundance and biomass in subseafloor sediment. Proc. Natl. Acad. Sci. U.S.A. 2012;109:16213-16216.
  57. Mohamed J., Bruno F., Eric G., Philippe O. Microbial diversity and adaptation to high hydrostatic pressure in deep-sea hydrothermal vents prokaryotes. Extremophiles. 2015;19:721-740.
  58. Casillo A., Parrilli E., Tutino M. L., Corsaro M. M. The outer membrane glycolipids of bacteria from cold environments: isolation, characterization, and biological activity. FEMS Microbiol. Ecol. 2019;95. fiz094.
  59. Holst O. Chemical structure of the core region of lipopolysaccharides. An update. Trends Glycosci. Glycotechnol. 2002;14:87-103.
  60. Ieranò T., Silipo A., Nazarenko E. L., Gorshkova R. P., Ivanova E. P., Garozzo D., Sturiale L., Lanzetta R., Parrilli M., Molinaro A. Against the rules: a marine bacterium, Loktanella rosea, possesses a unique lipopolysaccharide. Glycobiology. 2010;20(5):586-593.
  61. Tomshich S. V., Kokoulin M. S., Kalinovsky A. I., Komandrova N. A., Nedashkovskaya O. I. Structure of the O-specific polysaccharide from a marine bacterium Echinicola vietnamensis KMM 6221T. Carbohydr. Res. 2015;402:1-5.
  62. Tomshich S. V., Kokoulin M. S., Kalinovsky A. I., Komandrova N. A., Nedashkovskaya O. I. Structure of the O-specific polysaccharide from a marine bacterium Echinicola pacifica KMM 6172T containing 2,3-diacetamido-2,3-dideoxy-D-glucuronic acid. Carbohydr. Res. 2016;425:22-27.
  63. Pither M. D., Mantova G., Scaglione E., Pagliuca C., Colicchio R., Vitiello M., Chernikov O. V., Hua K.-F., Kokoulin M. S., Silipo A., Salvatore P., Molinaro A., De Lorenzo F. The unusual lipid A structure and immunoinhibitory activity of LPS from marine bacteria Echinicola pacifica KMM 6172T and Echinicola vietnamensis KMM 6221T. Microorganisms. 2021;9(12). 2552.
  64. Tomshich S. V., Kokoulin M. S., Kalinovskiy A. I., Nedashkovskaya O. I., Komandrova N. A. Structure of the O-specific polysaccharide from a marine bacterium Cellulophaga algicola. Carbohydr. Res. 2017;443/444:68-72.
  65. Tomshich S. V., Komandrova N. A., Nedashkovskaya O. I., Widmalm G., Perepelov A. V., Shashkov A. S. Structure of acidic O-specific polysaccharide from the marine bacterium Cellulophaga baltica. Russ. J. Bioorg. Chem. 2007;33:83-87.
  66. Perepelov A. V., Shashkov A. S., Tomshich S. V., Komandrova N. A., Nedashkovskaya O. I. A pseudoaminic acid-containing O-specific polysaccharide from a marine bacterium Cellulophaga fucicola. Carbohydr. Res. 2007;342(10):1378-1381.
  67. Staaf M., Weintraub A., Widmalm G. Structure determination of the O-antigenic polysaccharide from the enteroinvasive Escherichia coli O136. Eur. J. Biochem. 1999;263(3):656-661.
  68. Perepelov A. V., Shashkov A. S., Tomshich S. V., Komandrova N. A., Nedashkovskaya O. I. Structure of the O-specific polysaccharide from a marine bacterium Cellulophaga pacifica containing rarely occurred sugars, Fuc4NAc and ManNAcA. Carbohydr. Res. 2013;372:69-72.
  69. Erbel P. J., Barr K., Gao N., Gerwig G. J., Rick P. D., Gardner K. H. Identification and biosynthesis of cyclic enterobacterial common antigen in Escherichia coli. J. Bacteriol. 2003;185(6):1995-2004.
  70. Vinogradov E. V., Knirel Y. A., Thomas-Oates J.E., Shashkov A. S., L’vov V. L. The structure of the cyclic enterobacterial common antigen (ECA) from Yersinia pestis. Carbohydr. Res. 1994;258:223-232.
  71. Tomshich S. V., Kokoulin M. S., Kalinovsky A. I., Nedashkovskaya O. I., Komandrova N. A. Structure of the O-specific polysaccharide from a marine bacterium Cellulophaga tyrosinoxydans. Carbohydr. Res. 2015;413:1-4.
  72. Cirella R., Pagliuca Ch., Pither M. D., Scaglione E., Nedashkovskaya O. I., Chernikov O. V., Hua K.-F., Colicchio R., Vitiello M., Kokoulin M. S., Silipo A., Salvatore P., Molinaro A., Di Lorenzo F. Pushing the boundaries of structural heterogeneity with the lipid A of marine bacteria Cellulophaga. ChemBioChem. 2023;24(10). e202300183.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Pain. 1. Structure of VOCs I. zobellii KM 231T

Download (101KB)
Indexing metadata
3. Fig. 2. Lipid structures of E. vietnamensis KM 6221T and E. pacifica KMM 6172T

Download (155KB)
Indexing metadata
4. Pain. 3. The structure of lipids A of C. algicola COM 630T, C. baltica NO 15840T and C. tyrosinoxydans EM41T

Download (157KB)
Indexing metadata

Copyright (c) 2024 Russian Academy of Sciences