Skip to main content

Advertisement

SpringerLink
Log in

Sea foam-associated pathogenic bacteria along the west coast of India

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Anthropogenic activities release effluents containing nutrients and pathogenic bacteria that change the characteristics of coastal ecosystems. An important type of marine pollution which has occurred in 3 different states in India during 2019 is sea foam. Sea foam was found on Hole beach, Goa (Lat: 15.404° N, Long: 73.787° E), where nutrients (NO3− = 137 μM and organic nitrogen = 121 μM) from a garbage dumpyard are released directly via streams/gutters to coastal waters. This resulted in a bloom of the diatom Thalassiosira pseudonana, associated with high concentration of total organic carbon and fucoxanthin. Decay of this bloom along with strong agitation due to rocks and wave action resulted in sea foam. We isolated foam-associated bacteria and identified pathogenic bacteria including Enterobacter cancerogenus through 16S rRNA gene sequencing. Such foam-associated pathogenic bacteria, could be antibiotic resistant, and may have adverse effects on human health. This can also hamper the tourism industry of a small state like Goa that relies heavily on tourism.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Abbott, S. L., & Janda, J. M. (1997). Enterobacter cancerogenus (“Enterobacter taylorae”): infections associated with severe trauma or crush injuries. American Journal of Clinical Pathology, 107(3), 359–361.

    CAS  Google Scholar 

  • Anderson, D. M., Glibert, P. M., & Burkholder, J. M. (2002). Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries, 25(4), 704–726.

    Google Scholar 

  • Bätje, M., & Michaelis, H. (1986). Phaeocystis pouchetii blooms in the east Frisian coastal waters (German Bight, North Sea). Marine Biology, 93(1), 21–27.

    Google Scholar 

  • Batz, M. B., Hoffmann, S., & Morris, J. G. (2012). Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. Journal of Food Protection, 75(7), 1278–1291.

    Google Scholar 

  • Caballero, M. A., Jallet, D., Shi, L., Rithner, C., Zhang, Y., & Peers, G. (2016). Quantification of chrysolaminarin from the model diatom Phaeodactylum tricornutum. Algal Research, 20, 180–188.

    Google Scholar 

  • Chandrasekaran, S., Venkatesh, B., & Lalithakumari, D. (1998). Transfer and expression of a multiple antibiotic resistance plasmid in marine bacteria. Current Microbiology, 37(5), 347–351.

    CAS  Google Scholar 

  • Craig, D., Ireland, R. J., & Bärlocher, F. (1989). Seasonal variation in the organic composition of seafoam. Journal of Experimental Marine Biology and Ecology, 130(1), 71–80.

    CAS  Google Scholar 

  • Ruwandeepika, H.A.D.,  Jayaweera, T.S.P., Bhowmick, P.P., Karunasagar, I., Bossier, P., & Defoirdt, T. (2012). Pathogenesis, virulence factors and virulence regulation of vibrios belonging to the Harveyi clade. Reviews in Aquaculture, 4(2), 59–74.

  • Delétoile, A., Decré, D., Courant, S., Passet, V., Audo, J., Grimont, P., & Brisse, S. (2009). Phylogeny and identification of Pantoea species and typing of Pantoea agglomerans strains by multilocus gene sequencing. Journal of Clinical Microbiology, 47(2), 300–310.

    Google Scholar 

  • Demir, T., Baran, G., Buyukguclu, T., Sezgin, F. M., & Kaymaz, H. (2014). Pneumonia due to Enterobacter cancerogenus infection. Folia Microbiologica, 59(6), 527–530.

    CAS  Google Scholar 

  • Dickson, A. G., Sabine, C. L., & Christian, J. R. (2007). Guide to best practices for ocean CO2 measurements. North Pacific Marine Science Organization.PICES Special Publication 3, pp. 191.

  • Durbin, E. G. (1974). Studies on the Autecology of the marine diatom Thalassiosira Nordenskiöldii cleve. 1. the influence of daylength, light intensity, and temperature on growth 1. Journal of Phycology, 10(2), 220–225.

    Google Scholar 

  • Eberlein, K., Leal, M. T., Hammer, K. D., & Hickel, W. (1985). Dissolved organic substances during a Phaeocystis pouchetii bloom in the German Bight (North Sea). Marine Biology, 89(3), 311–316.

    CAS  Google Scholar 

  • Ettema, R., Johnson, J. K., & Schaefer, J. A. (1989). Foam-initiated ice covers on small rivers and streams: an observation. Cold Regions Science and Technology, 16(1), 95–99.

    Google Scholar 

  • Ferrari, V. C., & Hollibaugh, J. T. (1999). Distribution of microbial assemblages in the Central Arctic Ocean Basin studied by PCR/DGGE: analysis of a large data set. Hydrobiologia, 401, 55–68, 1999.

  • Fisenko, A. I. (2004). A new long-term on site clean-up approach applied to non-point sources of pollution. Water, Air, and Soil Pollution, 156(1), 1–27.

  • Gobalakrishnan, R., Sivakumar, K., Sethubathi, G. V., & Kannan, L. (2014). Seafoam bacteria from the Havelock island of the Andamans, India. Indian Journal of Marine Science, 43, 1562–1565.

    Google Scholar 

  • Grasshoff, P. (1983). Methods of seawater analysis. Verlag Chemie. FRG, 419, 61–72.

    Google Scholar 

  • Guerrini, F., Mazzotti, A., Boni, L., & Pistocchi, R. (1998). Bacterial-algal interactions in polysaccharide production. Aquatic Microbial Ecology, 15(3), 247–253.

    Google Scholar 

  • Guo, F., Wang, Z. P., Yu, K., & Zhang, T. (2015). Detailed investigation of the microbial community in foaming activated sludge reveals novel foam formers. Scientific Reports, 5, 7637.

    CAS  Google Scholar 

  • Guzmán, H. M., Cortés, J., Glynn, P. W., & Richmond, R. H. (1990). Coral mortality associated with dinoflagellate blooms in the eastern Pacific (Costa Rica and Panama). Marine Ecology Progress Series, 60, 299–303.

  • Hallegraeff, G. M. (1993). A review of harmful algal blooms and their apparent global increase. Phycologia, 32(2), 79–99.

    Google Scholar 

  • Harris, A. S. D., Medlin, L. K., Lewis, J., & Jones, K. J. (1995). Thalassiosira species (Bacillariophyceae) from a Scottish sea-loch. European Journal of Phycology, 30(2), 117–131.

    Google Scholar 

  • Hasle, G. R. (1970). Some species of the centric diatom genus Thalassiosira studied in the light and electron microscopes. Nova Hedwigia. Beiheft, 31, 557–559.

    Google Scholar 

  • Johnson, B. D., Zhou, X., Parrish, C. C., Wangersky, P. J., & Kerman, B. R. (1989). Fractionation of particulate matter, the trace metals Cu, Cd, and Zn, and lipids in foam and water below Niagara Falls. Journal of Great Lakes Research, 15(2), 189–196.

    CAS  Google Scholar 

  • Kamalanathan, M., Chiu, M. H., Bacosa, H., Schwehr, K., Tsai, S. M., Doyle, S., ... & Sylvan, J. B. (2019). Role of polysaccharides in diatom Thalassiosira pseudonana and its associated bacteria in hydrocarbon presence. Plant physiology, 180(4), 1898-1911.

  • Kent, M. L., Whyte, J. N. C., & LaTrace, C. (1995). Gill lesions and mortality in seawater pen-reared Atlantic salmon Salmo salar associated with a dense bloom of Skeletonema costatum and Thalassiosira species. Diseases of Aquatic Organisms, 22(1), 77–81.

    Google Scholar 

  • Kesaulya, I., Leterme, S. C., Mitchell, J. G., & Seuront, L. (2008). The impact of turbulence and phytoplankton dynamics on foam formation, seawater viscosity and chlorophyll concentration in the eastern English Channel. Oceanologia, 50 (2), 167–182

  • Kisluk, G., & Yaron, S. (2012). Presence and persistence of Salmonella enterica serotype Typhimurium in the phyllosphere and rhizosphere of spray-irrigated parsley. Applied and Environmental Microbiology, 78(11), 4030–4036.

    CAS  Google Scholar 

  • Koehn, R. D. (1982). Fungi isolated from sea foam collected at North Padre Island Beaches. The Southwestern Naturalist, 27(1), 17–21.

  • Kotloff, K. L., Nataro, J. P., Blackwelder, W. C., Nasrin, D., Farag, T. H., Panchalingam, S., Wu, Y., Sow, S. O., Sur, D., Breiman, R. F., & Faruque, A. S. (2013). Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. The Lancet, 382(9888), 209–222.

    Google Scholar 

  • Kurata, N., Vella, K., Hamilton, B., Shivji, M., Soloviev, A., Matt, S., ... & Perrie, W. (2016). Surfactant-associated bacteria in the near-surface layer of the ocean. Scientific Reports, 6(1), 1-8.

  • Kurian, S., Roy, R., Repeta, D. J., Gauns, M., Shenoy, D. M., Suresh, T., Sarkar, A., Narvenkar, G., Johnson, C. G., & Naqvi, S. W. A. (2012). Seasonal occurrence of anoxygenic photosynthesis in Tillari and Selaulim reservoirs, Western India. Biogeosciences, 9, 2485–2495.

    CAS  Google Scholar 

  • Kuznetsova, M., & Lee, C. (2002). Dissolved free and combined amino acids in nearshore seawater, sea surface microlayers and foams: influence of extracellular hydrolysis. Aquatic Sciences, 64(3), 252–268.

    CAS  Google Scholar 

  • Lane, D. J. (1991). 16S/23S rRNA sequencing. In: STACKEBRANDT, E.; GOODFELLOW, M., (Eds.). Nucleic acid techniques in bacterial systematics, (pp 115-175). New York: John Wiley and Sons.

  • Letscher, R. T., Hansell, D. A., Carlson, C. A., Lumpkin, R., & Knapp, A. N. (2013). Dissolved organic nitrogen in the global surface ocean: distribution and fate. Global Biogeochemical Cycles, 27(1), 141–153.

    CAS  Google Scholar 

  • López-Cortés, D. J., Núñez-Vázquez, E. J., Band-Schmidt, C. J., Gárate-Lizárraga, I., Hernández-Sandoval, F. E., & Bustillos-Guzmán, J. J. (2015). Mass fish die-off during a diatom bloom in the Bahía de La Paz, Gulf of California. Hidrobiológica, 25(1), 39–48.

  • Sarkar S.K., Satpathy, K.K., Jonathan, M.P., Bhattacharya, A.,Alam, A., Chatterjee, M., et al. (2012). Persistent Organic Pollutants (POPs) in Sediments and Biota in Coastal Environments of India. In: Lichtfouse E., Schwarzbauer J., Robert D. (eds) Environmental Chemistry for a Sustainable World. Environmental Chemistry for a Sustainable World. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2442-6_10.

  • Lightner, D. V. (1993). Diseases of cultured penaeid shrimp. CRC Handbook of Mariculture, 1, 393–486.

    Google Scholar 

  • López-Cortés, D. J., Núñez-Vázquez, E. J., Band-Schmidt, C. J., Gárate-Lizárraga, I., Hernández-Sandoval, F. E., & Bustillos-Guzmán, J. J. (2015). Mass fish die-off during a diatom bloom in the Bahía de La Paz, Gulf of California. Hidrobiológica, 25(1), 39–48.

    Google Scholar 

  • Madhupratap, M., Sawant, S., & Gauns, M. (2000). A first report on a bloom of the marine prymnesiophycean, Phaeocystis globosa from the Arabian Sea. Oceanologica Acta, 23(1), 83–90.

  • Madrange, L., Chaboury, P., Ferrandon, O., Mazet, M., & Rodeaud, J. (1993). Study of the formation and stability of chemical foam on the Vienne river between Limoges and Confolens [Etude de la formation et de la stabilite des mousses chimiques de surface de la Vienne]. Revue des Sciences de l'eau/Journal of Water Science, 6(3), 315–334.

    CAS  Google Scholar 

  • Maloo, A., Borade, S., Dhawde, R., Gajbhiye, S. N., & Dastager, S. G. (2014). Occurrence and distribution of multiple antibiotic-resistant bacteria of Enterobacteriaceae family in waters of Veraval coast, India. Environmental and Experimental Botony, 12, 43–50.

    Google Scholar 

  • Maynard, N. G. (1968). Aquatic foams as an ecological habitat. Zeitschrift für Allgemeine Mikrobiologie, 8(2), 119–126.

    CAS  Google Scholar 

  • Mopper, K., Ramana, K. S., & Drapeau, D. T. (1995). The role of surface-active carbohydrates in the flocculation of a diatom bloom in a mesocosm. Deep Sea Research Part II: Topical Studies in Oceanography, 42(1), 47–73.

    CAS  Google Scholar 

  • Napolitano, G. E., & Richmond, J. E. (1995). Enrichment of biogenic lipids, hydrocarbons and PCBs in stream-surface foams. Environmental Toxicology and Chemistry: An International Journal, 14(2), 197–201.

    CAS  Google Scholar 

  • Overy, D. P., Berrue, F., Correa, H., Hanif, N., Hay, K., Lanteigne, M., Mquilian, K., Duffy, S., Boland, P., Jagannathan, R., Carr, G. S., Vansteeland, M., & Kerr, R. G. (2014). Sea foam as a source of fungal inoculum for the isolation of biologically active natural products. Mycology, 5(3), 130–144. https://doi.org/10.1080/21501203.2014.931893.

    Article  CAS  Google Scholar 

  • Paerl, H. W., & Huisman, J. (2008). Blooms like it hot. Science, 320(5872), 57–58.

    CAS  Google Scholar 

  • Pednekar, S. M., Matondkar, S. P., Gomes, H. D. R., Goes, J. I., Parab, S., & Kerkar, V. (2011). Fine-scale responses of phytoplankton to freshwater influx in a tropical monsoonal estuary following the onset of southwest monsoon. Journal of Earth System Science, 120(3), 545–556.

    Google Scholar 

  • Popovich, C. A., & Gayoso, A. M. (1999). Effect of irradiance and temperature on the growth rate of Thalassiosira curviseriata Takano (Bacillariophyceae), a bloom diatom in Bahía Blanca estuary (Argentina). Journal of Plankton Research, 21(6), 1101–1110.

    Google Scholar 

  • Prasad, A. K., Nienow, J. A., & Lochner, E. (2018). Thalassiosira mala (Bacillariophyta), a potentially harmful, marine diatom from Chilka Lake and other coastal localities of Odisha, India: nomenclature, frustule morphology and global biogeography. Journal of Biosciences, 43(1), 59–74.

    Google Scholar 

  • Radchenko, I. G., Shevchenko, V. P., Kravchishina, M. D., Il’inskii, V. V., Georgiev, A. P., Tolstikov, A. V., & Ilyash, L. V. (2018). The first record of thalassiosira angulata (Bacillariophyceae) bloom in the White Sea: spatial distribution and associated species. Moscow University Biological Sciences Bulletin, 73(4), 217–221.

    Google Scholar 

  • Rahlff, J., Stolle, C., Giebel, H. A., Brinkhoff, T., Ribas-Ribas, M., Hodapp, D., & Wurl, O. (2017). High wind speeds prevent formation of a distinct bacterioneuston community in the sea-surface microlayer. FEMS Microbiology Ecology, 93(5).

  • Rahlff, J., Herlemann, D., Giebel, H. A., Mustaffa, N. I. H., Wurl, O., & Stolle, C. (2019). Marine foams represent compressed sea-surface microlayer with distinctive bacterial communities. bioRxiv, 820696.

  • Roveillo, Q., Dervaux, J., Wang, Y., Rouyer, F., Zanchi, D., Seuront, L., & Elias, F. (2020). Trapping of swimming microalgae in foam. Journal of the Royal Society Interface, 17(168), 20200077.

    CAS  Google Scholar 

  • Ruzicka, K., Gabriel, O., Bletterie, U., Winkler, S., & Zessner, M. (2009). Cause and effect relationship between foam formation and treated wastewater effluents in a transboundary river. Physics and Chemistry of the Earth, Parts A/B/C, 34(8-9), 565–573.

    Google Scholar 

  • Saha, D., & LaRocque, R. C. (2013). Cholera and other vibrios. In Hunter's Tropical Medicine and Emerging Infectious Disease, (9th edn.), 43, 448–453.

  • Sambrook, H. C., Fritsch, E. F.,  Maniatis, T. (1989). Molecular cloning: a laboratory manual. Cold Spring Harbor, NY. No.Ed. 2 pp.xxxviii + 1546 pp

  • Satpute, S. K., Banpurkar, A. G., Dhakephalkar, P. K., Banat, I. M., & Chopade, B. A. (2010). Methods for investigating biosurfactants and bioemulsifiers: a review. Critical Reviews in Biotechnology, 30(2), 127–144.

    CAS  Google Scholar 

  • Schilling, K., & Zessner, M. (2011). Foam in the aquatic environment. Water Research, 45(15), 4355–4366.

    CAS  Google Scholar 

  • Seitzinger, S. P., Kroeze, C., Bouwman, A. F., Caraco, N., Dentener, F., & Styles, R. V. (2002). Global patterns of dissolved inorganic and particulate nitrogen inputs to coastal systems: Recent conditions and future projections. Estuaries, 25(4), 640–655.

    CAS  Google Scholar 

  • Servais, P., & Passerat, J. (2009). Antimicrobial resistance of fecal bacteria in waters of the Seine river watershed (France). Science of the Total Environment, 408(2), 365–372.

    CAS  Google Scholar 

  • Seuront, L., Vincent, D., & Mitchell, J. G. (2006). Biologically induced modification of seawater viscosity in the Eastern English Channel during a Phaeocystis globosa spring bloom. Journal of Marine Systems, 61(3-4), 118–133.

    Google Scholar 

  • Shetye, S. S., Kurian, S., Naik, H., Gauns, M., Chndrasekhararao, A. V., Kumar, A., & Naik, B. (2019). Variability of organic nitrogen and its role in regulating phytoplankton in the eastern Arabian Sea. Marine Pollution Bulletin, 141, 550–560.

    CAS  Google Scholar 

  • Subrahmanyan, R. (1946). A systematic account of the marine plankton diatoms of the Madras coast. In Proceedings of the Indian Academy of Sciences-Section B, 24(4), 85-197. Springer India.

  • Subrahmanyan, R. (1968). The dinophyceae of the Indian seas. Part I. Genus Ceratium Schrank. The Marine Biological Association of India, 2, 1–129.

    Google Scholar 

  • Tomas, C. R. (1997). Identifying marine phytoplankton. Elsevier.Academic Press, pp.858. https://doi.org/10.1016/B978-0-12-693018-4.X5000-9

  • Tsyban, A. V. (1971). Marine bacterioneuston. Journal of the Oceanographical Society of Japan 27(2):56–66.

  • Van Heukelem, L. (2002). HPLC phytoplankton pigments: Sampling, laboratory methods, and quality assurance procedures. In: Mueller, J., Fargion, G. (Eds.), Ocean Optics Protocols for Satellite Ocean Color Sensor, Revision 3, Volume 2, Chapter 16, NASA Technical Memorandum 2002–2004, 258–268.

  • Velimirov, B. (1982). Sugar and lipid components in sea foam near kelp beds. Marine Ecology, 3(2), 97–107.

    CAS  Google Scholar 

  • Ward, P. B. (1966). Fatty acids in three plankton organisms. M.S. Thesis, Florida State University, Tallahassee, Florida. 38 pp.

  • Weinthal, D. M., Barash, I., Panijel, M., Valinsky, L., Gaba, V., & Manulis-Sasson, S. (2007). Distribution and replication of the pathogenicity plasmid pPATH in diverse populations of the gall-forming bacterium Pantoea agglomerans. Applied and Environmental Microbiology, 73(23), 7552–7561.

    CAS  Google Scholar 

  • Wilson, W. B., & Collier, A. (1972). The production of surface active material by marine phytoplankton cultures. Journal of Marine Research, 30, 15–26.

    Google Scholar 

  • Zhang, Z., Yu, Y. X., Jiang, Y., Wang, Y. G., Liao, M. J., Rong, X. J., Wang, K., Zhang, H., & Chen, J. (2019). First report of isolation and complete genome of Vibrio rotiferianus strain SSVR1601 from cage-cultured black rockfish (Sebastes schlegelii) associated with skin ulcer. Journal of Fish Diseases, 42(5), 623–630.

    CAS  Google Scholar 

  • Ẑutić, V., Ćosović, B., Marčenko, E., Bihari, N., & Kršinić, F. (1981). Surfactant production by marine phytoplankton. Marine Chemistry, 10, 505–520. https://doi.org/10.1016/0304-4203(81)90004-9.

    Article  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Director CSIR-National Institute of Oceanography for encouraging this work.

Funding

This work was carried out under the CSIR funded project MLP1802. This is NIO contribution no-6645.

Author information

Authors and Affiliations

  1. CSIR-National Institute of Oceanography, Donapaula, Goa, 403004, India

    Suhas S. Shetye, Mandar Bandekar, Kuniyil Nandakumar, Siby Kurian, Mangesh Gauns, Anil Pratihary, S. Sai Elangovan, Bhagyashri R. Naik, Sethu Lakshmi & V. K. Aswathi

  2. Svalbard Integrated Arctic Earth Observing System (SIOS), SIOS Knowledge Centre, Svalbard Science Centre, P.O. Box 156, N-9171, Longyearbyen, Svalbard, Norway

    Shridhar Jawak

Authors
  1. Suhas S. Shetye
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mandar Bandekar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kuniyil Nandakumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Siby Kurian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mangesh Gauns
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shridhar Jawak
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Anil Pratihary
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. S. Sai Elangovan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Bhagyashri R. Naik
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Sethu Lakshmi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. V. K. Aswathi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Suhas S. Shetye.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(MP4 5050 kb)

ESM 2

(JPG 2734 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shetye, S.S., Bandekar, M., Nandakumar, K. et al. Sea foam-associated pathogenic bacteria along the west coast of India. Environ Monit Assess 193, 27 (2021). https://doi.org/10.1007/s10661-020-08783-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-020-08783-4

Keywords

Search

Navigation