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Vertical and temporal microbial community patterns in a meromictic coastal lake influenced by the Straits of Messina upwelling system

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Abstract

The vertical and temporal dynamics of total picoplankton, heterotrophic nanoflagellates and ciliates were monitored monthly from May 2002 to April 2003, along with environmental parameters, in Lake Faro, a meromictic coastal basin characterized by a permanently anoxic monimolimnion and sulfide-rich bottom waters. A two-layer discrimination was delineated in the water column of the lake, based on the correlations between environmental and biological descriptors and on the ciliated protozoa community composition. The latter showed a clear zonation pattern along the water column with two main recognizable facies: a superficial and a deep one. Choreotrichida and Strombidiida dominated the upper facies nearly throughout the study period, while Tintinnida were only found in summer months. The mixotrophic cyclotrichid Myrionecta rubra was also frequently observed in the upper facies. Typical of the deep facies was the occurrence of Pleuronematida (Cyclidium sp.) and of flagellates of the order Cryptomonadida (Chilomonas sp.), which were the main potential picoplankton grazers during a summer bloom of photosynthetic sulfur bacteria. Sporadic inputs of Levantine Intermediate Waters (LIW) from the upwelling system of the Straits of Messina, although limited to the mixolimnion, clearly affected the physical and chemical environment, as well as the microbial biomass and the ciliated protozoa assemblage composition, all along the water column of the lake, suggesting that meromictic basins, although strongly stratified, may experience perturbation effects from the surface down to the bottom, with important consequences on their biogeochemical cycles and on their ecology.

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References

  • Acosta Pomar, L., V. Bruni, F. Decembrini, G. Giuffrè & T. L. Maugeri, 1988. Distribution and activity of picophytoplankton in a brackish environment. Progress in Oceanography 21: 129–138.

    Article  Google Scholar 

  • Bloem, J. & M. J. B. Bär-Gilissen, 1989. Bacterial activity and protozoan grazing potential in a stratified lake. Limnology and Oceanography 34: 297–309.

    Google Scholar 

  • Bloem, J., M. J. B. Bär-Glissen & T. E. Cappenberg, 1986. Fixation, counting, and manipulation of heterotrophic nanoflagellates. Applied and Environmental Microbiology 52: 1266–1272.

    PubMed  Google Scholar 

  • Bockstahler, K. R. & D. W. Coats, 1993. Spatial and temporal aspects of mixotrophy in Chesapeake Bay dinoflagellates. Journal of Eukaryotic Microbiology 40: 49–60.

    Article  Google Scholar 

  • Børsheim K.Y. & G. Bratbak (1987) Cell volume to cell carbon conversion factors for a bacterivorous Monas sp. enriched from seawaters. Marine Ecology Progress Series 36: 171–175.

    Article  Google Scholar 

  • Brugnano, C., G. Zagami & A. Granata, 2006. Preliminary data on egg production rates of Pseudocyclops xiphophorus Wells, 1967 from brackish Lake Faro (North-Eastern Sicily). Chemistry and Ecology 22: 191–195.

    Article  Google Scholar 

  • Brandt, P., A. Rubino, W. Alpers & J. O. Backhaus, 1997. Internal waves in the Strait of Messina studied by a numerical model and synthetic aperture radar images from the ERS 1/2 satellites. Journal of Physical Oceanography 27: 648–663.

    Article  Google Scholar 

  • Camacho, A., J. Erez, A. Chicote, M. Florín, M. M. Squires, C. Lehmann & R. Bachofen, 2001. Microbial microstratification, inorganic carbon photoassimilation and dark carbon fixation at the chemocline of the meromictic Lake Cadagno (Switzerland) and its relevance to the food web. Aquatic Sciences 63: 91–106.

    Article  CAS  Google Scholar 

  • Carey, P. G., 1992. Marine interstitial ciliates—an illustrated key. Natural History Museum Publications, London.

    Google Scholar 

  • Carlson, R. E., 1977. A trophic state index for lakes. Limnology and Oceanography 22: 361–369.

    CAS  Google Scholar 

  • Clesceri, L. S., A. E. Greenberg & A. D. Eaton (eds), 1999. Standard methods for the examination of water and wastewater. In American Waterworks Association and Water Environment Federation, 1268 pp.

  • Cortese, G. & E. De Domenico, 1990. Some considerations on the Levantine Intermediate Water distribution in the Straits of Messina. Bollettino di Oceanologia Teorica ed Applicata VIII: 197–204.

    Google Scholar 

  • De Domenico, E., 1987. Caratteristiche Fisiche e Chimiche delle Acque nello Stretto di Messina. Documents et Travaux 11: 225–237.

    Google Scholar 

  • Defant, A., 1961. Physical Oceanography, Vol 2. Pergamon Press, New York, 598 pp.

  • Eccleston-Parry, J. D. & B. S. C. Leadbeater, 1995. Regeneration of phosphorus and nitrogen by four species of heterotrophic nanoflagellates feeding on three nutritional states of a single bacterial strain. Applied and Environmental Microbiology 61: 1033–1038.

    PubMed  CAS  Google Scholar 

  • Esteban, G., T. Fenchel & B. J. Finlay, 1995. Diversity of free living morphospecies in the ciliate genus Metopus. Archiv für Protistenkunde 146: 137–164.

    Google Scholar 

  • Esteban, G., B. E. Guhl, K. J. Clarke, T. M. Embley & B. J. Finlay, 1993. Cyclidium porcatum n. sp.: a free living anaerobic scuticociliate containing a stable complex of hydrogenosomes, eubacteria and archaeobacteria. European Journal of Protistology 29: 262–270.

    Google Scholar 

  • Fenchel, T. & B. J. Finlay, 1992. Production of methane and hydrogen by anaerobic ciliates containing symbiotic methanogens. Archives of Microbiology 157: 475–480.

    CAS  Google Scholar 

  • Fenchel, T., G. M. King & T. H. Blackburn, 1998. The ecophysiology of mineral cycling. In Bacterial Biogeochemistry. Academic Press, 4–42.

  • Fenchel, T., L. D. Kristensen & L. Rasmussen, 1990. Water column anoxia: vertical zonation of planktonic protozoa. Marine Ecology Progress Series 62: 1–10.

    Article  Google Scholar 

  • Fenchel, T., T. Perry & A. Thane, 1977. Anaerobiosis and symbiosis with bacteria in free-living ciliates. Journal of Protozoology 24: 154–163.

    PubMed  CAS  Google Scholar 

  • Fenchel, T. & N. B. Ramsing, 1992. Identification of sulphate-reducing ectosymbiotic bacteria from anaerobic ciliates using 16s rRNA binding oligonucleotide probes. Archives of Microbiology 158: 394–397.

    Article  PubMed  CAS  Google Scholar 

  • Finlay, B. J., S. C. Maberly & G. F. Esteban, 1996. Spectacular abundance of ciliates in anoxic pond water: contribution of symbiont photosynthesis to host respiratory oxygen requirements. FEMS Microbiology Ecology 20: 229–235.

    Article  CAS  Google Scholar 

  • Gabriel, K. R., 1971. The biplot graphic display of matrices with application to principal component analysis. Biometrika 58: 453–467.

    Article  Google Scholar 

  • Genovese, S. & G. Magazzù, 1969. Manuale d’Analisi per le Acque Salmastre. La Editrice Universitaria, Messina.

    Google Scholar 

  • Gustafson, D. E. J., D. K. Stoecker, M. D. Johnson, W. F. Van Heukelem & K. Sneider, 2000. Cryptophyte algae are robbed of their organelles by the marine ciliate Mesodinium rubrum. Nature 405: 1049–1052.

    Article  PubMed  CAS  Google Scholar 

  • Hotelling, H., 1933. Analysis of a complex of statistical variables into principal components. Journal of Educational Psychology 24: 417–441, 498–520.

    Article  Google Scholar 

  • Humayoun, S. B., N. Bano & J. T. Hollibaugh, 2003. Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Applied and Environmental Microbiology 69: 1030–1042.

    Article  PubMed  CAS  Google Scholar 

  • Jetten, M. S., O. Sliekers, M. Kuypers, T. Dalsgaard, L. van Niftrik, I. Cirpus, K. van de Pas-Schoonen, G. Lavik, B. Thamdrup, D. Le Paslier, H. J. Op den Camp, S. Hulth, L. P. Nielsen, W. Abma, K. Third, P. Engstrom, J. G. Kuenen, B. B. Jorgensen, D. E. Canfield, J. S. Sinninghe Damste, N. P. Revsbech, J. Fuerst, J. Weissenbach, M. Wagner, I. Schmidt, M. Schmid & M. Strous, 2003. Anaerobic ammonium oxidation by marine and freshwater planctomycete-like bacteria. Applied Microbiology and Biotechnology 63: 107–114.

    Article  PubMed  CAS  Google Scholar 

  • Kofoid, C. A. & S. A. Campbell, 1929. A conspectus of the marine and fresh-water Ciliata belonging to the suborder Tintinnoinea, with descriptions of new species principally from the Agassiz expedition to the Eastern Tropical Pacific 1904–1905. University of California Publication, Zoology 34: 1–403.

    Google Scholar 

  • Kofoid, C. A. & S. A. Campbell, 1939. The Ciliata: the Tintinnoinea. Reports on the scientific results of the expedition to the Eastern Tropical Pacific 1904–1905. Bulletin of the Museum of Comparative Zoology, Harvard 84: 1–473.

    Google Scholar 

  • Kosolapov, D. B., D. Yu. Rogozin, I. A. Gladchenko, A. I. Kopylov & E. E. Zakharova, 2003. Microbial sulfate reduction in a brackish meromictic steppe lake. Aquatic Ecology 37: 215–226.

    Article  CAS  Google Scholar 

  • Kress, N. & B. Herut, 2001. Spatial and seasonal evolution of dissolved oxygen and nutrients in the Southern Levantine Basin (Eastern Mediterranean Sea): chemical characterization of the water masses and inferences on the N:P ratios. Deep-Sea Research I 48: 2347–2372.

    Article  CAS  Google Scholar 

  • Krom, M. D., E. M. S. Woodward, B. Herut, N. Kress, P. Carbo, R. F. C. Mantoura, G. Spyres, T. F. Thingsted, P. Wassmann, C. Wexels-Riser, V. Kitidis, C. Law & G. Zodiatis, 2005. Nutrient cycling in the South East Levantine Basin of the Eastern Mediterranean: results from a phosphorus starved system. Deep-Sea Research II 52: 2879–2896.

    Article  Google Scholar 

  • Kuenen, J. G. & M. S. M. Jetten, 2001. Extraordinary anaerobic ammonium-oxidizing bacteria. ASM News 67: 456–463.

    Google Scholar 

  • Kuypers, M. M., A. O. Sliekers, G. Lavik, M. Schmid, B. B. Jorgensen, J. G. Kuenen, J. S. Sinninghen Damste, M. Strous & M. S. Jetten, 2003. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422: 608–611.

    Article  PubMed  CAS  Google Scholar 

  • Laybourn-Parry, J., J. Olver, A. Rogerson & P. L. Duvergé, 1990. The temporal and spatial patterns of protozooplankton abundance in a eutrophic temperate lake. Hydrobiologia 203: 99–110.

    Article  Google Scholar 

  • Lee, S. & J. A. Fuhrman, 1987. Relationship between biovolume and biomass of naturally derived marine bacterioplankton. Applied and Environmental Microbiology 53: 1298–1303.

    PubMed  CAS  Google Scholar 

  • Legendre, P. & L. Legendre, 1998. Principal components analysis. In Numerical Ecology. Elsevier, Amsterdam, 387–424.

  • Lehours, A.-C., C. Bardot, A. Thenot, D. Debroas & G. Fonty, 2005. Anaerobic microbial communities in Lake Pavin, a unique meromictic lake in France. Applied and Environmental Microbiology 71: 7389–7400.

    Article  PubMed  CAS  Google Scholar 

  • Lynn, D. H., 2003. The Ciliate Resource Archive. http://www.uoguelph.ca/~ciliates Accessed on 2007 Jan 20.

  • Macek, M., G. Vilaclara & A. Lugo, 1994. Changes in protozoan assemblage structure and activity in a stratified tropical lake. Marine Microbial Food Webs 8: 235–149.

    Google Scholar 

  • Madigan, M., S. S. Cox & R. A. Stegeman, 1984. Nitrogen fixation and nitrogenase activities in members of the family Rhodospirillaceae. Journal of Bacteriology 157: 73–78.

    PubMed  CAS  Google Scholar 

  • Marshall, S. M., 1969. Protozoa, Tintinnida. In Fraser, J. H. & V. K. Hansen (eds), Fiches D’identification Du Zooplankton. Conseil Permanent International pour l’Explanation de la Mer, Charlottenlund slot – Denmark, Sheets 117–127.

  • McDonough, R. J., R. W. Sanders, K. G. Porter & D. L. Kirchman, 1986. Depth distribution of bacterial production in a stratified lake with an anoxic hypolimnion. Applied and Environmental Microbiology 11: 1199–1204.

    Google Scholar 

  • Mulder, A., A. A. van de Graaf, L. A. Robertson & J. G. Kuenen, 1995. Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiology and Ecology 16: 177–183.

    Article  CAS  Google Scholar 

  • Nõges, T., I. Solovjova, 2005. The formation and dynamics of deep bacteriochlorophyll maximum in the temperate and partly meromictic Lake Verevi. Hydrobiologia 547: 73–81.

    Article  CAS  Google Scholar 

  • Norland, S., 1993. The relationship between biomass and volume of bacteria. In Kemp, P. F., B. F. Sherr, E. B. Sherr & J. Cole (eds) Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, Ann Arbor, London, Tokyo, 303–307.

    Google Scholar 

  • Norland, S., M. Heldal & O. Tumyr, 1987. On the relation between dry matter and volume of bacteria. Microbial Ecology 13: 95–101.

    Article  Google Scholar 

  • Park, J. S. & B. C. Cho, 2002. Active heterotrophic nanoflagellates in the hypoxic water-column of the eutrophic Masan Bay, Korea. Marine Ecology Progress Series 230: 35–45.

    Article  Google Scholar 

  • Parsons, T. R., M. Takahashi & B. Hargrave, 1977. Biological oceanographic processes. Pergamon, New York, 71–88.

    Google Scholar 

  • Peters, F., C. Marrassé, J. M. Gasol, M. M. Sala & L. Arin, 1998. Effects of turbulence on bacterial growth mediated through food web interactions. Marine Ecology Progress Series 172: 293–303.

    Article  Google Scholar 

  • Peters, F., C. Marrassé, H. Havskum, F. Rassoulzadegan, J. Dolan, M. Alcaraz & J. M. Gasol, 2002. Turbulence and the microbial food web: effects on bacterial losses to predation and on community structure. Journal of Plankton Research 24: 321–331.

    Article  Google Scholar 

  • Pimenov, N. V., I. I. Rusanov, O. V. Karnachuk, D. Yu. Rogozin, I. A. Bryantseva, O. N. Lunina, S. K. Yusupov, V. P. Parnachev & M. V. Ivanov, 2003. Microbial processes of the carbon and sulfur cycles in Lake Shira (Khakasia). Microbiology 72: 221–229.

    Article  CAS  Google Scholar 

  • Philips, S., H. J. Laanbroek & W. Verstraete, 2002. Origin, causes and effects of increased nitrite concentrations in aquatic environments. Reviews in Environmental Science & Biotechnology 1: 115–141.

    Article  CAS  Google Scholar 

  • Porter, K. G. & Y. S. Feig, 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography 25: 943–948.

    Google Scholar 

  • Poughon, L., C. G. Dussap & J. B. Gros, 1999. Dynamic model of a nitrifying fixed bed column: simulation of the biomass distribution of nitrosomonas and nitrobacter and of transient behaviour of the column. Bioprocesses Engineering 20: 209–221.

    CAS  Google Scholar 

  • Putt, M. & D. K. Stoecker, 1989. An experimentally determined carbon: volume ratio for marine “Oligotrichous” ciliates from estuarine and coastal waters. Limnology and Oceanography 34: 1097–1103.

    Article  Google Scholar 

  • Rodrigo, M. A., M. R. Miracle & E. Vicente, 2001. The meromictic Lake La Cruz (Central Spain). Patterns of stratification. Aquatic Science 63: 406–416.

    Article  Google Scholar 

  • Sherr, B. F., E. B. Sherr & T. Berman, 1983. Grazing, growth, and ammonium excretion rates of a heterotrophic microflagellate fed with four species of bacteria. Applied and Environmental Microbiology 45: 1196–1201.

    PubMed  Google Scholar 

  • Simon, M. & F. Azam, 1989. Protein content and protein synthesis rates of planktonic marine bacteria. Marine Ecology Progress Series 51: 201–213.

    Article  CAS  Google Scholar 

  • Sorokin, Y. I., 1970. Interrelations between sulphur and carbon turnover in meromictic lakes. Archiv für Hydrobiologie 66: 391–446.

    Google Scholar 

  • Sorokin, Y. I. & N. Donato, 1975. On the carbon and sulphur metabolism in the meromictic Lake Faro (Sicily). Hydrobiologia 47: 241–252.

    Article  CAS  Google Scholar 

  • Trüper, H. G. & S. Genovese, 1968. Characterization of photosynthetic sulfur bacteria causing red water in Lake Faro (Messina, Sicily). Limnology and Oceanography 13: 225–232.

    Google Scholar 

  • Utermöhl, H. Zur Vervollkommnung der quantitativen Phytoplankton Methodik, 1958. Internationale Vereinigung für theoretische und angewandte Limnologie. Mitteilungen 9: 1–38.

  • Vercelli, F., 1925. Il Regime delle Correnti e delle Maree nello Stretto di Messina. Commissione Internazionale del Mediterraneo, Campagne della R. Nave Marsigli negli anni 1922 e 1923, 209 pp.

  • Verity, P. G. & M. E. Sieracki, 1993. Use of color image analysis and epifluorescence microscopy to measure plankton biomass. In Kemp, P. F., B. F. Sherr, E. B. Sherr & J. J. Cole (eds), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, Ann Arbor, London, Tokyo, 327–337.

    Google Scholar 

  • Wahlund, T. M. & M. T. Madigan, 1993. Nitrogen fixation by the thermophilic green sulfur bacterium chlorobium tepidum. Journal of Bacteriology 175: 474–478.

    PubMed  CAS  Google Scholar 

  • Zehr, J. P., R. W. Harvey, R. S. Oremland, J. E. Cloern, L. H. George & J. L. Lane, 1987. Big Soda Lake (Nevada). 1. Pelagic bacterial heterotrophy and biomass. Limnology and Oceanography 32: 781–793.

    CAS  Google Scholar 

  • Zingel, P. & I. Ott, 2000. Vertical distribution of planktonic ciliates in strongly stratified temperate lakes. Hydrobiologia 435: 19–26.

    Article  Google Scholar 

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Acknowledgements

We thank Prof. G. Giuffrè of the University of Messina for his valuable assistance with this study. Thanks are due to T. Tanaka for the technical advice for epifluorescence microscopy. We are also grateful to Nino Donato for the assistance in field sampling and to Mary Ann McKay for her English language revision. The Go-Flo Bottle and the Zeiss Axioplan 2-Imaging® microscope system were kindly provided by the “Istituto per l’Ambiente Marino Costiero” (Messina).

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  1. Dipartimento di Biologia Animale ed Ecologia Marina, Facoltà di Scienze, Università degli Studi di Messina, Salita Sperone 31, S. Agata, 98166, Messina, Italy

    Alessandro Saccà, Letterio Guglielmo & Vivia Bruni

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  1. Alessandro Saccà
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Saccà, A., Guglielmo, L. & Bruni, V. Vertical and temporal microbial community patterns in a meromictic coastal lake influenced by the Straits of Messina upwelling system. Hydrobiologia 600, 89–104 (2008). https://doi.org/10.1007/s10750-007-9179-x

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