Abstract
Plankton represent a nutrient-rich reservoir capable of enriching Vibrio species, which can include human pathogens, at higher densities than the surrounding water column. To better understand the relationship between vibrios and plankton, the partitioning of culturable vibrios, on TCBS, between free living and plankton associated (63–200- and >200-μm-size fractions) was monitored over a 1-year period in coastal waters of Georgia, USA. Seasonal changes in the total Vibrio concentration were then compared with changes in environmental parameters as well as changes in the relative composition of the plankton community. Using univariate analyses, Vibrio concentrations were strongly associated with temperature, especially when those vibrios were plankton associated (R2=0.69 and 0.88 for the water and both plankton fractions; respectively) (P<0.01). Multivariate general linear models revealed that Vibrio concentrations in the plankton fractions were also correlated to shifts in the relative abundance of specific plankton taxa. In the 63–200-μm fraction, Vibrio concentrations were inversely associated with copepods, cyanobacteria and diatoms. In the >200-μm fraction, Vibrio concentrations were positively associated with copepods and negatively associated with decapod larvae. Our results confirm the role of temperature in Vibrio seasonality and highlight an important and independent role for plankton composition in explaining seasonal changes in Vibrio concentration.
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References
Baffone W, Tarsi R, Pane L, Campana R, Repetto B, Mariottini GL et al. (2006). Detection of free-living and plankton-bound vibrios in coastal waters of the Adriatic Sea (Italy) and study of their pathogenicity-associated properties. Environ Microbiol 8: 1299–1305.
Colwell RR, Grimes DJ . (1984). Vibrio diseases of marine fish populations. Helgol Mar Res 37: 265–287.
Colwell RR, Huq A, Islam MS, Aziz KMA, Yunus M, Khan NH et al. (2003). Reduction of cholera in Bangladeshi villages by simple filtration. Proc Natl Acad Sci USA 100: 1051–1055.
Eiler A, Gonzalez-Rey C, Allen S, Bertilsson S . (2007). Growth response of Vibrio cholerae and other Vibrio spp. to cyanobacterial dissolved organic matter and temperature in brackish water. FEMS Microbiol Ecol 60: 411–418.
Fandino LB, Riemann L, Steward GF, Long RA, Azam F . (2001). Variations in bacterial community structure during a dinoflagellate bloom analyzed by DGGE and 16 S rDNA sequencing. Aquat Microb Ecol 23: 119–130.
Grossart HP, Levold F, Allgaier M, Simon M, Brinkhoff T . (2005). Marine diatom species harbour distinct bacterial communities. Environ Microbiol 7: 860–873.
Heidelberg JF, Heidelberg KB, Colwell RR . (2002a). Bacteria of the γ-subclass proteobacteria associated with zooplankton in Chesapeake Bay. Appl Environ Microbiol 68: 5498–5507.
Heidelberg JF, Heidelberg KB, Colwell RR . (2002b). Seasonality of Chesapeake Bay Bacterioplankton species. Appl Environ Microbiol 68: 5488–5497.
Huq A, Xu B, Chowdhury MA, Islam MS, Montilla R, Colwell RR . (1996). A simple filtration method to remove plankton-associated Vibrio cholerae in raw water supplies in developing countries. Appl Environ Microbiol 62: 2508–2512.
Huq A, Colwell RR . (1996). Environmental factors associated with emergence of disease with special reference to cholera. East Mediterr Health J 2: 37–45.
Huq A, Sack RB, Nizam A, Longini IM, Nair GB, Ali A et al. (2005). Critical factors influencing the occurrence of Vibrio cholerae in the environment of Bangladesh. Appl Environ Microbiol 71: 4645–4654.
Huq A, Small EB, West PA, Huq MI, Rahman R, Colwell RR . (1983). Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl Environ Microbiol 45: 275–283.
Huq A, West PA, Small EB, Huq MI, Colwell RR . (1984). 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 48: 420–424.
Lam C, Stang A, Harder T . (2008). Planktonic bacteria and fungi are selectively eliminated by exposure to marine macroalgae in close proximity. FEMS Microbiol Ecol 63: 283–291.
Lancelot C, Billen G . (1984). Activity of heterotrophic bacteria and its coupling to primary production during the spring phytoplankton bloom in the Southern Bight of the North Sea. Limnol Oceanogr 29: 721–730.
Lipp EK, Rivera ING, Gil AI, Espeland EM, Choopun N, Louis VR et al. (2003). Direct detection of Vibrio cholerae and ctxA in Peruvian Coastal water and plankton by PCR. Appl Environ Microbiol 69: 3676–3680.
Lipp EK, Rodriguez-Palacios C, Rose JB . (2001). Occurrence and distribution of the human pathogen Vibrio vulnificus in a subtropical Gulf of Mexico estuary. Hydrobiologia 460: 165–173.
Long RA, Azam F . (2001). Antagonistic interactions among Marine Pelagic Bacteria. Appl Environ Microbiol 67: 4975–4983.
Long RA, Rowley DC, Zamora E, Liu J, Bartlett DH, Azam F . (2005). Antagonistic interactions among marine bacteria impede the proliferation of Vibrio cholerae. Appl Environ Microbiol 71: 8531–8536.
Louis VR, Russek-Cohen E, Choopun N, Rivera ING, Gangle B, Jiang SC et al. (2003). Predictability of Vibrio cholerae in Chesapeake Bay. Appl Environ Microbiol 69: 2773–2785.
Massad G, Oliver JD . (1987). New selective and differential medium for Vibrio cholerae and Vibrio vulnificus. Appl Environ Microbiol 53: 2262–2264.
Middelboe M, Søndergaard M, Letarte Y, Borch NH . (1995). Attached and free-living bacteria: production and polymer hydrolysis during a diatom bloom. Microb Ecol 29: 231–248.
Morris Jr JG . (2003). Cholera and other types of vibriosis: a story of human Pandemics and Oysters on the half shell. Clin Infect Dis 37: 272–280.
Panicker G, Call DR, Krug MJ, Bej AK . (2004). Detection of pathogenic Vibrio spp. in shellfish by using multiplex PCR and DNA microarrays. Appl Environ Microbiol 70: 7436–7444.
Pfeffer C, Oliver JD . (2003). A comparison of thiosulphate-citrate-bile salts-sucrose(TCBS) agar and thiosulphate-chloride-iodide(TCI) agar for the isolation of Vibrio species from estuarine environments. Lett Appl Microbiol 36: 150–151.
Pfeffer CS, Hite MF, Oliver JD . (2003). Ecology of Vibrio vulnificus in estuarine waters of eastern North Carolina. Appl Environ Microbiol 69: 3526–3531.
Pinhassi J, Sala MM, Havskum H, Peters F, Guadayol O, Malits A et al. (2004). Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microbiol 70: 6753–6766.
Pomeroy LR, Wiebe WJ . (2001). Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol 23: 187–204.
Randa MA, Polz MF, Lim E . (2004). Effects of temperature and salinity on Vibrio vulnificus population dynamics as assessed by quantitative PCR. Appl Environ Microbiol 70: 5469–5476.
Riemann L, Steward GF, Azam F . (2000). Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl Environ Microbiol 66: 578.
Singh PK, Prasanna R, Jaiswal P . (2008). Cyanobacterial bioactive molecules-an overview of their toxic properties. Can J Microbiol 54: 701–717.
Sochard MR, Wilson DF, Austin B, Colwell RR . (1979). Bacteria associated with the surface and gut of marine copepods. Appl Environ Microbiol 37: 750–759.
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: 1977–1980.
Thomas KU, Joseph N, Raveendran O, Nair S . (2006). Salinity-induced survival strategy of Vibrio cholerae associated with copepods in Cochin backwaters. Mar Pollut Bull 52: 1425–1430.
Thompson FL, Iida T, Swings J . (2003a). Biodiversity of vibrios. Microbiol Mol Biol Rev 68: 403–431.
Thompson JR, Randa MA, Marcelino LA, Tomita-Mitchell A, Lim E, Polz MF . (2003b). Diversity and dynamics of a north Atlantic coastal Vibrio community. Appl Environ Microbiol 70: 4103–4110.
Verity PG, Alber M, Bricker SB . (2006). Development of hypoxia in well-mixed subtropical estuaries in the southeastern USA. Estuaries and coasts 29: 665–673.
Acknowledgements
This work was funded by the National Oceanic and Atmospheric Administration (NOAA) (Oceans and Human Health Initiative, Grant no. NA04OAR4600203). We thank the Georgia Department of Natural Resources (Coastal Research Division), especially our field coordinators, B Good, W Hughes and D Guadagnoli, for organizing monthly collection trips.
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Turner, J., Good, B., Cole, D. et al. Plankton composition and environmental factors contribute to Vibrio seasonality. ISME J 3, 1082–1092 (2009). https://doi.org/10.1038/ismej.2009.50
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DOI: https://doi.org/10.1038/ismej.2009.50
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