Wetlands Ecology and Management

, Volume 19, Issue 1, pp 109–119 | Cite as

Vibrio cholerae in waters of the Sunderban mangrove: relationship with biogeochemical parameters and chitin in seston size fractions

  • Rubén J. Lara
  • Sucharit B. Neogi
  • Mohammad S. Islam
  • Zahid H. Mahmud
  • Shafiqul Islam
  • Debasish Paul
  • Biniam B. Demoz
  • Shinji Yamasaki
  • Gopinath B. Nair
  • Gerhard Kattner
Original Paper

Abstract

Wetland dynamics are probably linked to cholera endemicity in South Asia. We focus on links between Vibrio cholerae abundance, chitin content and suspended particle load in size fractions of suspended particulate matter (SPM) along the salinity gradient of Sunderban mangrove waters. SPM decreased downstream, while salinity increased from 0.2 to 4. Particulate organic carbon (90 ± 25 μM) and nitrogen (9.1 ± 3.3 μM) highly correlated with SPM and turbidity, suggesting a significant contribution of fine particles to organic matter. Total chitin ranged 1–2 mg/l and decreased downstream. The distribution among size fractions of SPM, chitin and V. cholerae O1 (the bacterial serogroup mainly associated with cholera epidemics) was similar, with ~98% of the total in the fraction <20 μm. In comparison, the number of V. cholerae O1 attached to zooplankton and microplankton size classes >20 μm was almost negligible, in contrast to usual assumptions. Thus, microdetritus, nanoplankton and fungal cells in size classes <20 μm represent a chitinaceous substrate on which V. cholerae can grow and survive. Total bacteria, cultivable vibrios and V. cholera O1 increased 5–10 times downstream, together with salinity and nitrite concentration. Overall, nitrate and silicate concentrations were relatively constant (>22 μM N and 100 μM Si). However, nitrite increased ~9 times in the outer sector, reaching ~1.2 μM N, probably as a result of increased abundance of nitrate-reducing vibrios. A characterization of Vibrio habitats that takes account of the presence of nitrate-reducing bacteria could improve the understanding of both mangrove nitrogen cycling and cholera seasonality.

Keywords

Chitin Cholera Sunderban Tropical estuaries Vibrios 

References

  1. Adel MM (2005) Background state leading to arsenic accumulation in the Bengal basin groundwater. J Water Health 3:435–452PubMedGoogle Scholar
  2. APHA (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association (APHA), American Water Works Association (AWWA) & Water Environment Federation (WEF), Washington, DCGoogle Scholar
  3. Bhowmick R, Ghosal A, Chatterjee NS (2007) Effect of environmental factors on expression and activity of chitinase genes of vibrios with special reference to Vibrio cholerae. J Appl Microbiol 103:97–108CrossRefPubMedGoogle Scholar
  4. Biswas H, Dey M, Ganguly D, De TK, Ghosh S, Jana TK (2010) Comparative analysis of phytoplankton composition and abundance over a two-decade period at the land–ocean boundary of a tropical mangrove ecosystem. Estuaries Coasts 33:384–394CrossRefGoogle Scholar
  5. Brandhorst W (1959) Nitrification and denitrification in the eastern tropical North Pacific. J Cons Int Explor Mer 25:3–20Google Scholar
  6. Colwell RR, Huq A, Islam MS, Aziz KM, Yunus M, Khan NH, Mahmud A, Sack RB, Nair GB, Chakraborty J, Sack DA, Russek-Cohen E (2003) Reduction of cholera in Bangladeshi villages by simple filtration. Proc Natl Acad Sci USA 100:1051–1055CrossRefPubMedGoogle Scholar
  7. Dham VV, Menezes Heredia A, Wafar S, Wafar M (2002) Seasonal variations in uptake and in situ regeneration of nitrogen in mangrove waters. Limnol Oceanogr 47:241–254CrossRefGoogle Scholar
  8. Dittmar T, Lara RJ (2001) Driving forces behind nutrient and organic matter dynamics in a mangrove tidal creek in North Brazil. Est Coast Shelf Sci 52:249–259CrossRefGoogle Scholar
  9. Faruque SM, Sack DA, Sack RB, Colwell RR, Takeda Y, Nair GB (2003) Emergence and evolution of Vibrio cholerae O139. Proc Natl Acad Sci USA 100:1304–1309CrossRefPubMedGoogle Scholar
  10. Gallagher JT, Morris A, Dexter TM (1985) Identification of two binding sites for wheat-germ agglutinin on polylactosamine-type oligosaccharides. Biochem J 231:115–122PubMedGoogle Scholar
  11. Gebauer M (2007) Bangladesh: Wo der Klimawandel nach Salz schmeckt. Spiegel on-line 26. April 2007Google Scholar
  12. Gismervik I (1997) Implications of zooplankton stoichiometry on distribution of N and P among planktonic size fractions. J Plankton Res 19:343–356CrossRefGoogle Scholar
  13. Huq A, Colwell RR (1995) Vibrios in marine and estuarine environment. J Mar Biotechnol 3:60–63Google Scholar
  14. Ishimaru K, Akagawa-Matsushita M, Muroga K (1996) Vibrio ichthyoenteri sp. nov., a pathogen of Japanese flounder (Paralichthys olivaceus) larvae. Int J Syst Bacteriol 46:155–159CrossRefGoogle Scholar
  15. Islam MS, Drasar BS, Bradley DJ (1990) Long-term persistence of toxigenic Vibrio cholerae O1 in the mucilaginous sheath of a blue-green alga, Anabaena variabilis. J Trop Med Hyg 93:133–139PubMedGoogle Scholar
  16. Islam MS, Alam MJ, Khan SI, Huq A (1994a) Fecal pollution of freshwater environments in Bangladesh. Int J Environ Stud 46:161–165CrossRefGoogle Scholar
  17. Islam MS, Drasar BS, Sack RB (1994b) The aquatic flora and fauna as reservoirs of Vibrio cholerae: a review. J Diarrhoeal Dis Res 12:87–96PubMedGoogle Scholar
  18. Islam MS, Drasar BS, Sack RB (1994c) Probable role of blue-green algae in maintaining endemicity and seasonality of cholera in Bangladesh: a hypothesis. J Diarrhoeal Dis Res 12:245–256PubMedGoogle Scholar
  19. Islam MS, Siddika A, Khan MNH, Goldar MM, Sadique MA, Kabir A (2001) Microbiological analysis of tube-well water in a rural area of Bangladesh. Appl Environ Microbiol 67:3328–3330CrossRefPubMedGoogle Scholar
  20. Islam MS, Brooks A, Kabir MS, Jahid IK, Shafiqul Islam M, Goswami D, Nair GB, Larson C, Yukiko W, Luby S (2007) Faecal contamination of drinking water sources of Dhaka city during the 2004 flood in Bangladesh and use of disinfectants for water treatment. J Appl Microbiol 103:80–87CrossRefGoogle Scholar
  21. Kattner G (1999) Storage of dissolved inorganic nutrients in seawater: poisoning with mercuric chloride. Mar Chem 67:61–66CrossRefGoogle Scholar
  22. Kattner G, Becker H (1991) Nutrients and organic nitrogenous compounds in the marginal ice zone of the Fram Strait. J Mar Syst 2:385–394CrossRefGoogle Scholar
  23. Keyhani NO, Roseman S (1999) Physiological aspects of chitin catabolism in marine bacteria. Biochim Biophys Acta 1473:108–122Google Scholar
  24. Koch R (1884) An address on cholera and its bacillus. Br Med J 6:453–459CrossRefGoogle Scholar
  25. Lara RJ, Neogi SB, Islam S, Mahmud ZH, Yamasaki S, Nair GB (2009) Influence of estuarine dynamics and catastrophic climatic events on Vibrio distribution in the Karnaphuli estuary, Bangladesh. EcoHealth 6:279–286CrossRefPubMedGoogle Scholar
  26. Lara RJ, Islam MS, Yamasaki S, Neogi SB, Nair GB (in press) Aquatic ecosystems, human health and ecohydrology. In: E. Wolanski, D. McLusky (eds) Treatise on estuarine and coastal science.“Ecohydrology and restoration”,Vol. 10 (L. Chícharo, M. Zalewski (eds.)). Elsevier, AmsterdamGoogle Scholar
  27. Laws EA, Popp B.N, Bidigare RR, Riebesell U, Burkhardt S, Wakeham SG (2001) Controls on the molecular distribution and carbon isotopic composition of alkenones in certain haptophyte algae. Geochem Geophys Geosyst 2. doi:10.1029/2000GC000057
  28. Lio-Po GD, Leaño EM, Peñaranda MMD, Villa-Franco AU, Sombito CD, Guanzon NG Jr (2005) Anti-luminous Vibrio factors associated with the ‘green water’ grow-out culture of the tiger shrimp Penaeus monodon. Aquaculture 250:1–7CrossRefGoogle Scholar
  29. Lobitz B, Beck L, Huq A, Wood B, Fuchs G, Faruque ASG, Colwell RR (2000) Climate and infectious disease: use of remote sensing for detection of Vibrio cholerae by indirect measurement. Proc Natl Acad Sci USA 97:1438–1443CrossRefPubMedGoogle Scholar
  30. MacFarlane GT, Herbert RA (1982) Nitrate dissimilation by Vibrio spp. isolated from estuarine sediments. J Gen Microbiol 128:2463–2468Google Scholar
  31. Meibom KL, Blokesch M, Dolganov NA, Wu CY, Schoolnik GK (2005) Chitin induces natural competence in Vibrio cholerae. Science 310:1824–1827CrossRefPubMedGoogle Scholar
  32. Miller CJ, Drasar BS, Feachem RG (1982) Cholera and estuarine salinity in Calcutta and London. Lancet 29:1216–1218CrossRefGoogle Scholar
  33. Mirza MMQ (1998) Diversion of the Ganges water at Farakka and its effects on salinity in Bangladesh. Environ Manag 22:711–722CrossRefGoogle Scholar
  34. Moloney CL, Field JG (1991) The size-based dynamics of plankton food webs. I. a simulation model of carbon and nitrogen flows. J Plankton Res 13:1003–1038CrossRefGoogle Scholar
  35. Montgomery MT, Welschmeyer NA, Kirchman DL (1990) A simple assay for chitin: application to sediment trap samples from the subarctic Pacific. Mar Ecol Prog Ser 64:301–308 CrossRefGoogle Scholar
  36. OCHA (2007) Bangladesh Cyclone Sidr. United Nations Office for the Coordination of Humanitarian Affairs. http://ochaonline.un.org/News/Emergencies/Bangladesh/tabid/2707/Default.aspx. Accessed on December 3, 2007
  37. Rameshkumar N, Sproer C, Lang E, Nair S (2010) Vibrio mangrovi sp.nov., a diazotrophic bacterium isolated from mangrove-associated wild rice (Poteresia coarctata Tateoka). FEMS Microbiol Lett 307:35–40CrossRefPubMedGoogle Scholar
  38. Svitil AL, Ni Chadhain SM, Moore JA, Kirchman DL (1997) Chitin degradation proteins produced by the marine bacterium Vibrio harveyi growing on different forms of chitin. Appl Environ Microbiol 63:408–413PubMedGoogle Scholar
  39. Tamplin ML, Gauzens AL, Huq A, Sack DA, Colwell RR (1990) Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl Environ Microbiol 56:1977–1980PubMedGoogle Scholar
  40. Udden SM, Zahid MS, Biswas K, Ahmad QS, Cravioto A, Nair GB, Mekalanos JJ, Faruque SM (2008) Acquisition of classical CTX prophage from Vibrio cholerae O141 by El Tor strains aided by lytic phages and chitin-induced competence. Proc Natl Acad Sci USA 105:11951–11956CrossRefPubMedGoogle Scholar
  41. UNEP (2007) Fast melting glaciers from rising temperatures expose millions in himalaya to devastating floods and water shortages. UNEP-ROAP News Release 07/10.http://www.unep.org/Documents.Multilingual/Default.asp?DocumentID=512&ArticleID=5600&l=en
  42. Watkins WD, Cabelli VJ (1985) Effect of fecal pollution on Vibrio parahaemolyticus densities in an estuarine environment. Appl Environ Microbiol 49:1307-1313PubMedGoogle Scholar
  43. West PA, Colwell RR (1984) Identification and classification of Vibrionaceae: an overview. In: RR Colwell (ed) Vibrios in the environment, New York, John Wiley, pp 285–363Google Scholar
  44. Wichern F (2004) Fungi vs bacteria: their different roles in decomposition of organic matter. soils are alive newsletter, Vol. 3 Nr 3. http://www.soilhealth.see.uwa.edu.au/fungi_vs_bacteriacomponents/
  45. Wolf AT (2001) Water and human security. J Contemp Water Res Educ 118:29Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Rubén J. Lara
    • 1
  • Sucharit B. Neogi
    • 2
    • 4
  • Mohammad S. Islam
    • 2
  • Zahid H. Mahmud
    • 2
  • Shafiqul Islam
    • 2
  • Debasish Paul
    • 2
  • Biniam B. Demoz
    • 3
  • Shinji Yamasaki
    • 4
  • Gopinath B. Nair
    • 5
  • Gerhard Kattner
    • 6
  1. 1.Leibniz Centre for Tropical Marine EcologyBremenGermany
  2. 2.International Centre for Diarrhoeal Disease Research, BangladeshDhakaBangladesh
  3. 3.Institute of Environmental and Animal Hygiene and Veterinary MedicineUniversity of HohenheimStuttgartGermany
  4. 4.Graduate School of Life and Environmental SciencesOsaka Prefecture UniversitySakaiJapan
  5. 5.National Institute of Cholera and Enteric DiseasesKolkataIndia
  6. 6.Ecological ChemistryAlfred Wegener Institute for Polar and Marine ResearchBremerhavenGermany

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