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Biogeochemical patterns and microbial processes in the Eastern Mediterranean Deep Water of Ionian Sea

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Abstract

Microbial processes involved in water biogeochemistry are linked to physical and chemical variability of water masses. While the occurrence of hydrological changes in the Eastern Mediterranean Sea has been documented, its effects on microbial dynamics and processes have been poorly investigated. An interdisciplinary survey was carried out in November 2011 to depict recent scenarios in the Ionian Mediterranean Sea. This study provides a snapshot of the hydrology and biogeochemistry of this basin, with particular emphasis on the abyssal waters, where two cores of the Eastern Mediterranean Deep Water, both of Adriatic origin, were found. The first core, located at about 3000 m, overlies the second one, which has a recent origin. Both water masses have Adriatic origin and the upper one is older than the lower one. A novel approach has been adopted to relate changes in microbial abundance and metabolism to new thermohaline and biogeochemical findings. A close relationship between surface processes driven by air–sea interaction, microbial variables, physical and chemical parameters (nutrients, dissolved organic carbon and oxygen) was observed. Being intimately coupled to DOC patterns, the microbial respiratory activity was likely the most responsive microbial parameter to hydrological changes, confirming this variable as a sentinel of environmental changes.

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Abbreviations

LAP:

Leucine aminopeptidase

β-GLU:

Beta glucosidase

AP:

Alkaline phosphatase

PHP:

Prokaryotic heterotrophic production

ETSa:

Electron transport system assay

PA:

Prokaryotic abundance

PB:

Prokaryotic biomass

cell LAP:

Cell-specific LAP

cell β-GLU:

Cell-specific beta glucosidase

cell AP:

Cell-specific AP

cell-PHP:

Cell-specific PHP

AW/ISW:

Atlantic water/ionian surface water

CIW/LIW:

Cretan intermediate water/Levantine intermediate water

TMW:

Transitional Mediterranean water

EMDWold :

Old Eastern Mediterranean Deep Water

EMDWnew :

New Eastern Mediterranean Deep Water

References

  • Ahmed, S. I., R. A. Kenner & F. D. King, 1976. Preservation of enzyme activity in marine plankton by low-temperature freezing. Marine Chemistry 4: 133–139.

    Article  CAS  Google Scholar 

  • Artale, V., D. Iudicone, R. Santoleri, V. Rupolo, S. Marullo & F. D’Ortenzio, 2002. Role of surface fluxes in ocean general circulation models using satellite sea surface temperature: validation of and sensitivity to the forcing frequency of the Mediterranean thermohaline circulation. Journal of Geophysical Research 107: C8.

    Article  Google Scholar 

  • Azzaro, M., R. La Ferla & F. Azzaro, 2006. Microbial respiration in the aphotic zone of the Ross Sea (Antarctica). Marine Chemistry 99(1–4): 199–209.

    Article  CAS  Google Scholar 

  • Azzaro, M., R. La Ferla, G. Maimone, L. S. Monticelli, R. Zaccone & G. Civitarese, 2012. Prokaryotic dynamics and heterotrophic metabolism in a deep convection site of Eastern Mediterranean Sea (the Southern Adriatic Pit). Continental Shelf Research 44: 106–118.

    Article  Google Scholar 

  • Baltar, F., J. Arístegui, E. Sintes, H. M. van Haken, J. M. Gasol & G. J. Herndl, 2009. Prokaryotic extracellular enzyme activity in relation to biomass production and respiration in the meso- and bathypelagic waters of the (sub) tropical Atlantic. Environmental Microbiology 11(8): 1998–2014.

    Article  CAS  PubMed  Google Scholar 

  • Baltar, F., J. Arístegui, J. M. Gasol, E. Sintes, H. M. van Haken & G. J. Herndl, 2010. High dissolved extracellular enzymatic activity in the deep central Atlantic Ocean. Aquatic Microbial Ecology 58: 287–302.

    Article  Google Scholar 

  • Bensi, M., A. Rubino, V. Cardin, D. Hainbucher & I. Mancero- Mosquera, 2013. Structure and variability of the abyssal water masses in the Ionian Sea in the period 2003-2010. Journal of Geophysical Research 118: 1–13.

    Google Scholar 

  • Beuvier, J., F. Sevault, M. Hermann, H. Kontoyiannis, W. Ludwig, M. Rixen, E. Stanev, K. Béranger & S. Somot, 2010. Modeling the Mediterranean Sea interannual variability during 1961–2000: Focus on the Eastern Mediterranean Transient. Journal of Geophysical Research. https://doi.org/10.1029/2009jc005950.

    Google Scholar 

  • Brankart, J. M., 1994. The MODB Local Quality Control. University of Liège, Liège.

    Google Scholar 

  • Bratbak, G., 1985. Bacterial biovolume and biomass estimation. Applied and Environmental Microbiology 49: 1488–1493.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cardin, V., M. Bensi & M. Pacciaroni, 2011. Variability of water mass properties in the last two decades in the Southern Adriatic Sea with emphasis on the period 2006–2009. Continental Shelf Research 31: 951–965.

    Article  Google Scholar 

  • Cardin, V., G. Civitarese, D. Hainbucher, M. Bensi & A. Rubino, 2015. Thermohaline properties in the Eastern Mediterranean in the last three decades: is the basin returning to the pre-EMT situation? Ocean Science 11: 53–66.

    Article  Google Scholar 

  • Caruso, G., 2010. Leucine aminopeptidase, beta-glucosidase and alkaline phosphatase activity rates and their significance in Carbon and Phosphorus cycles in some coastal Mediterranean sites. Marine Drugs 8(4): 916–940.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castellari, S., N. Pinardi & K. Leaman, 2000. Simulation of water mass formation processes in the Mediterranean sea: influence of the time frequency of the atmospheric forcing. Journal of Geophysical Research 105(C10): 24157–24181.

    Article  Google Scholar 

  • Christensen, J. P., T. T. Packard, F. Q. Dortch, H. J. Minas, J. C. Gascard, C. Richez & P. C. Garfield, 1989. Carbon oxidation in the deep Mediterranean Sea: evidence for dissolved organic carbon source. Global Biogeochemical Cycles 3: 315–335.

    Article  CAS  Google Scholar 

  • Civitarese, G., M. Gačić, M. Lipizer & G. L. Eusebi Borzelli, 2010. On the impact of the Bimodal Oscillating System (BiOS) on the biogeochemistry and biology of the Adriatic and Ionian Seas (Eastern Mediterranean). Biogeosciences 7: 3987–3997.

    Article  CAS  Google Scholar 

  • Coll, M., C. Piroddi, J. Steenbeek, K. Kaschner, F. Ben, R. Lasram, J. Aguzzi, E. Ballesteros, C. Bianchi, J. Corbera, T. Dailianis, R. Danovaro, M. Estrada, C. Froglia, B. S. Galil, J. M. Gasol, R. Gertwagen, J. Gil, F. Guilhaumon, K. Kesner-Reyes, M. Kitsos, A. Koukouras, N. Lampadariou, E. Laxamana, C. M. López-Fé de la Cuadra, H. K. Lotze, D. Martin, D. Mouillot, D. Oro, S. Raicevich, J. R. Barile, J. I. Saiz-Salinas, C. San Vicente, S. Somot, J. Templado, X. Turon, D. Vafidis, R. Villanueva & E. Voultsiadou, 2010. The biodiversity of the Mediterranean Sea: Estimates, patterns, and threats. PLoS ONE 5(8): 1–36.

    Article  Google Scholar 

  • Del Giorgio, P. A. & J. J. Cole, 1998. Bacterial Growth Efficiency in natural aquatic systems. Annual Review of Ecology, Evolution, and Systematics 29: 503–541.

    Article  Google Scholar 

  • Demirov, E. & N. Pinardi, 2002. Simulation of the Mediterranean Sea circulation from 1979 to 1993: Part I, The interannual variability. Journal of Marine Systems 33–34: 23–50.

    Article  Google Scholar 

  • Fry, J. C., 1990. Direct methods and biomass estimation. Methods in Microbiology 22: 41–85.

    Article  Google Scholar 

  • Gačić, M., G. L. E. Borzelli, G. Civitarese, V. Cardin & S. Yari, 2010. Can internal processes sustain reversals of the ocean upper circulation?: The Ionian Sea example. Geophysical Research Letters. https://doi.org/10.1029/2010GL043216.

    Google Scholar 

  • Gačić, M., G. Civitarese, G. L. E. Borzelli, V. Kovačević, P.-M. Poulain, A. Theocharis, M. Menna, A. Catucci & N. Zarokanellos, 2011. On the relationship between the decadal oscillations of the Northern Ionian Sea and the salinity distributions in the Eastern Mediterranean. Journal of Geophysical Research. https://doi.org/10.1029/2011JC007280.

    Google Scholar 

  • Grasshoff, K., K. Kremling & M. Ehrhardt, 1999. Methods of Seawater Analysis. Wiley-Vch Verlag, Weinheim.

    Book  Google Scholar 

  • Hainbucher, D., A. Rubino, V. Cardin, T. Tanhua, K. Schroeder & M. Bensi, 2014. Hydrographic situation during cruise M84/3 and P414 (spring) in the Mediterranean Sea. Ocean Science 10: 669–682.

    Article  Google Scholar 

  • Hansell, D. A., 2005. Dissolved organic carbon reference material program. Eos Transactions American Geophysical Union 86(35): 318.

    Article  Google Scholar 

  • Hoppe, H. G., 1983. Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Marine Ecology Progress Series l l. https://doi.org/10.3354/meps011299.

    Google Scholar 

  • Hoppe, H. G., 2003. Phosphatase activity in the sea. Hydrobiologia 493: 187–200.

    Article  CAS  Google Scholar 

  • Hoppe, H. G. & S. Ulrich, 1999. Profile of ectoenzymes in the Indian Ocean: phenomena of phosphatase activity in the mesopelagic zone. Aquatic Microbial Ecology 19: 139–148.

    Article  Google Scholar 

  • Kenner, R. A. & S. I. Ahmed, 1975. Measurements of electron transport activities in marine phytoplankton. Marine Biology 33(2): 119–127.

    Article  CAS  Google Scholar 

  • Kirchman, D. L., 1993. Leucine incorporation as a measure of biomass production by heterotrophic bacteria. In Kemp, P. F., B. F. Sherr, E. B. Sherr & J. J. Cole (eds), Handbook of Methods in Aquatic Microbial Ecology. Lewis, Ann Arbor: 509–512.

    Google Scholar 

  • Kirchman, D., E. K’Nees & R. Hodson, 1985. Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Applied and Environmental Microbiology 49: 599–607.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Klein, B., W. Roether, N. Kress, B. B. Manca, M. Ribera d’Alcalà, E. Souvermezoglou, A. Theocharis, G. Civitarese & A. Luchetta, 2003. Accelerated oxygen consumption in eastern Mediterranean deep waters following the recent changes in thermohaline circulation. Journal of Geophysical Research 108: 8107.

    Article  Google Scholar 

  • La Ferla, R. & M. Azzaro, 2001. Microbial respiration in the Levantine Sea: evolution of the oxidative processes in relation to the main Mediterranean water masses. Deep-Sea Research Part I: Oceanographic Research Papers 48(10): 2147–2159.

    Article  Google Scholar 

  • La Ferla, R. & M. Azzaro, 2004. Metabolic CO2 production in the Mediterranean Sea: a study basin for estimating carbon budget in the sea. Scientia Marina 68(suppl. 1): 57–64.

    Article  Google Scholar 

  • La Ferla, R., M. Azzaro & G. Chiodo, 1996. Microbial respiratory activity in the euphotic zone of the Mediterranean Sea. New Microbiologica 19(3): 243–250.

    PubMed  Google Scholar 

  • La Ferla, R., M. Azzaro, G. Civitarese & M. Ribera d’Alcalà, 2003. Distribution patterns of carbon oxidation in the Eastern Mediterranean Sea: evidence of changes in remineralization processes. Journal of Geophysical Research 108: 8111.

    Article  Google Scholar 

  • La Ferla, R., F. Azzaro, M. Azzaro, G. Caruso, F. Decembrini, M. Leonardi, G. Maimone, L. S. Monticelli, F. Raffa, C. Santinelli, R. Zaccone & M. Ribera d’Alcalà, 2005. Microbial contribution to carbon biogeochemistry in the Mediterranean Sea: variability of activities and biomass. Journal of Marine Systems 57: 146–166.

    Article  Google Scholar 

  • La Ferla, R., M. Azzaro, G. Caruso, L. S. Monticelli, G. Maimone, R. Zaccone & T. T. Packard, 2010. Prokaryotic abundance and heterotrophic metabolism in the deep Mediterranean Sea. Advances in Limnology and Oceanography 1(1): 143–166.

    Article  Google Scholar 

  • La Ferla, R., G. Maimone, M. Azzaro, F. Conversano, C. Brunet, A. S. Cabral & R. Paranhos, 2012. Vertical distribution of the prokaryotic cell size in the Mediterranean Sea. Helgoland Marine Research 66: 635–650.

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lionello, P., 2012. The climate of the Mediterranean region. From the past to the future. Elsevier, Amsterdam.

    Google Scholar 

  • Loferer-Kroßbacher, M., J. Klima & R. Psenner, 1998. Determination of bacterial cell ¨dry mass by transmission electron microscopy and densitometric image analysis. Applied and Environmental Microbiology 64: 688–694.

    PubMed  PubMed Central  Google Scholar 

  • Luna, G. M., S. Bianchelli, F. Decembrini, E. De Domenico, R. Danovaro & A. Dell’Anno, 2012. The dark portion of the Mediterranean Sea is a bioreactor of organic matter cycling. Global Biogeochemical Cycles 26(2): GB2017.

    Article  Google Scholar 

  • Malanotte-Rizzoli, P., B. B. Manca, M. Ribera d’Alcala, A. Theocharis, S. Brenner, G. Budillon & E. Ozsoy, 1999. The Eastern Mediterranean in the 80s and in the 90s: the big transition in the intermediate and deep circulations. Dynamics of Atmospheres and Oceans 29: 365–395.

    Article  Google Scholar 

  • Malanotte-Rizzoli, P., V. Artale, G. L. Borzelli-Eusebi, S. Brenner, A. Crise, M. Gačić, N. Kress, S. Marullo, M. Ribera d’Alcalà, S. Sofianos, T. Tanhua, A. Theocharis, M. Alvarez, Y. Ashkenazy, A. Bergamasco, V. Cardin, S. Carnie, G. Civitarese, F. D’Ortenzio, J. Font, E. Garcia-Ladona, J. M. Garcia-Lafuente, A. Gogou, M. Gregoire, D. Hainbucher, H. Kontoyannis, V. Kovacevic, E. Kraskapoulou, G. Kroskos, A. Incarbona, M. G. Mazzocchi, M. Orlic, E. Ozsoy, A. Pascual, P.-M. Poulain, W. Roether, A. Rubino, K. Schroeder, J. Siokou-Frangou, E. Souvermezoglou, M. Sprovieri, J. Tintoré & G. Triantafyllou, 2014. Physical forcing and physical/biochemical variability of the Mediterranean Sea: a review of unresolved issues and directions for future research. Ocean Science 10: 281–322.

    Article  CAS  Google Scholar 

  • Manca, B. B., V. Ibello, M. Pacciaroni, P. Scarazzato & A. Giorgetti, 2006. Ventilation of deep waters in the Adriatic and Ionian Seas following changes in thermohaline circulation of the Eastern Mediterranean. Climate Research 31(2–3): 239–256.

    Article  Google Scholar 

  • Massana, R., J. P. Gasol, P. K. Bjørnsen, N. Blackburn, A. Hanström, S. Hietanen, B. H. Hygum, J. Kuparinen & C. Pedrós-Alió, 1997. Measurement of bacterial size via image analysis of epifluorescence preparations: description of an inexpensive system and solutions to some of the most common problems. Scientia Marina 61(3): 397–407.

    Google Scholar 

  • Mertens, C. & F. Shott, 1998. Interannual variability of deepwater formation in the northwestern Mediterranean. Journal of Physical Oceanography 28: 1410–1424.

    Article  Google Scholar 

  • Packard, T. T., 1971. The measurement of respiratory electron transport activity in marine phytoplankton. Journal of Geophysical Research 29: 235–244.

    Google Scholar 

  • Packard, T. T., 1985. Measurement of respiratory electron transport activity of microplankton. In Jannasch, H. W. & P. Williams (eds), Advances in Aquatic Microbiology. Academic Press, New York: 207–261.

    Google Scholar 

  • Packard, T. T., A. H. Devol & F. D. King, 1975. The effect of temperature on the respiratory electron transport system in marine plankton. Deep-Sea Research Part II 22(4): 237–249.

    CAS  Google Scholar 

  • Pollard, P. C. & D. J. W. Moriarty, 1984. Validity of the tritiated thymidine methods for estimating bacterial growth rates: measurement of isotope dilution during DNA synthesis. Applied and Environmental Microbiology 48: 1076–1083.

    CAS  PubMed  PubMed Central  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.

    Article  Google Scholar 

  • Roether, W., B. B. Manca, B. Klein, D. Bregant, D. Georgopoulos, V. Beitzel, V. Kovačević & A. Luchetta, 1996. Recent changes in Eastern Mediterranean deep waters. Science 271: 333–335.

    Article  CAS  Google Scholar 

  • Rubino, A. & D. Hainbucher, 2007. A large abrupt change in the abyssal water masses of the eastern Mediterranean. Geophysical Research Letters 34: L23607.

    Google Scholar 

  • Santinelli, C., 2015. DOC in the Mediterranean Sea. In Hansell, D. A. & C. A. Carlson (eds), Biogeochemistry of Marine Dissolved Organic Matter, 2nd ed. Academic Press, Burlington: 579–608.

    Chapter  Google Scholar 

  • Santinelli, C., L. Nannicini & A. Seritti, 2010. DOC dynamics in the meso and bathypelagic layers of the Mediterranean Sea. Deep-Sea Research Part II 57: 1446–1459.

    Article  CAS  Google Scholar 

  • Schlitzer, R., 2015. Ocean Data View. http://odv.awi.de.

  • Seritti, A., B. B. Manca, C. Santinelli, E. Murru, A. Boldrin & L. Nannicini, 2003. Relationships between dissolved organic carbon (DOC) and water mass structures in the Ionian Sea (winter 1999). Journal of Geophysical Research 108: 8112.

    Article  Google Scholar 

  • Smethie, W. M. & R. A. Fine, 2001. Rates of North Atlantic Deep Water formation calculated from chlorofluorocarbon inventories. Deep-Sea Research Part I 48(1): 189–215.

    Article  CAS  Google Scholar 

  • Smith, D. C. & F. Azam, 1992. A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Marine Microbial Food Webs 6: 107–114.

    Google Scholar 

  • Sparnocchia, S., G. P. Gasparini, K. Schroeder & M. Borghini, 2011. Oceanographic conditions in the NEMO region during the KM3NeT project (April 2006–May 2009). Nuclear Instruments and Methods in Physics Research Section A 626: S87–S90.

    Article  Google Scholar 

  • Takahashi, T., W. S. Broecker & S. Langer, 1985. Redfield ratio based on chemical data from isopycnal surfaces. Journal of Geophysical Research 90: 6907–6924.

    Article  CAS  Google Scholar 

  • Tamburini, C., J. Garcin & A. Bianchi, 2002. Role of deep-sea bacteria in organic matter mineralization and adaptation to hydrostatic pressure conditions in the NW Mediterranean Sea. Aquatic Microbial Ecology 32: 209–218.

    Article  Google Scholar 

  • Theocharis, A., E. Balopoulos, S. Kioroglou, H. Kontoyiannis & A. Iona, 1999. A synthesis of the circulation and hydrography of the South Aegean Sea and the Straits of the Cretan Arc (March 1994–January 1995). Progress in Oceanography 44: 469–509.

    Article  Google Scholar 

  • Tian, C., D. Deibel, R. Rivkin & A. Vézina, 2004. Biogenic carbon and nitrogen export in a deep-convection region: simulations in the Labrador Sea. Deep-Sea Research 51(3): 413–437.

    Article  CAS  Google Scholar 

  • Van Wambeke, F., P. Catala, M. Pujo-Pay & P. Lebaron, 2011. Vertical and longitudinal gradients in HNA-LNA cell abundances and cytometric characteristics in the Mediterranean Sea. Biogeosciences 8: 1853–1863.

    Article  Google Scholar 

  • Wu, P. & K. Haines, 1996. Modeling the dispersal of Levantine Intermediate Water and its role in Mediterranean deep water formation. Journal of Geophysical Research 101: 6591–6607.

    Article  Google Scholar 

  • Zaccone, R., L. S. Monticelli, A. Seritti, C. Santinelli, M. Azzaro, A. Boldrin, R. La Ferla & M. Ribera d’Alcalà, 2003. Bacterial processes in the intermediate and deep layers of the Ionian Sea in winter 1999: vertical profiles and their relationship to the different water masses. Journal of Geophysical Research 108(C9): 8117.

    Article  Google Scholar 

  • Zaccone, R., G. Caruso, M. Azzaro, F. Azzaro, E. Crisafi, F. Decembrini, E. De Domenico, M. De Domenico, R. La Ferla, M. Leonardi, A. Lo Giudice, G. Maimone, M. Mancuso, L. Michaud, L. S. Monticelli, F. Raffa, G. Ruggeri & V. Bruni, 2010. Prokaryotic activities and abundance in pelagic areas of the Ionian Sea. Chemistry and Ecology 26(S1): 169–197.

    Article  Google Scholar 

  • Zaccone, R., A. Boldrin, G. Caruso, R. La Ferla, G. Maimone, C. Santinelli & M. Turchetto, 2012. Enzymatic activities and prokaryotic abundance in relation to organic matter along a West-East Mediterranean transect (TRANSMED cruise). Microbial Ecology 64(1): 54–66.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The Authors are grateful to Dr. Valeria Micale (CNR-IAMC Messina) for her accurate revision of English language as well as to the Editor and the anonymous referees for their valuable suggestions.

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Placenti, F., Azzaro, M., Artale, V. et al. Biogeochemical patterns and microbial processes in the Eastern Mediterranean Deep Water of Ionian Sea. Hydrobiologia 815, 97–112 (2018). https://doi.org/10.1007/s10750-018-3554-7

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