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Microbial Ecology

, Volume 67, Issue 3, pp 501–519 | Cite as

Role of Prokaryotic Biomasses and Activities in Carbon and Phosphorus Cycles at a Coastal, Thermohaline Front and in Offshore Waters (Gulf of Manfredonia, Southern Adriatic Sea)

  • L. S. MonticelliEmail author
  • G. Caruso
  • F. Decembrini
  • C. Caroppo
  • F. Fiesoletti
Microbiology of Aquatic Systems

Abstract

The Western areas of the Adriatic Sea are subjected to inputs of inorganic nutrients and organic matter that can modify the trophic status of the waters and consequently, the microbiological processes involved in the carbon and phosphorus biogeochemical cycles, particularly in shallow coastal environments. To explore this topic, a survey was carried out during the spring of 2003 in a particular hydrodynamic area of the Gulf of Manfredonia, where the potential (P) and real (R) rates of four different microbial exoenzymatic activities (EEA) (α [αG] and ß glucosidases [ßG], leucine aminopeptidase [LAP], and alkaline phosphatase [AP]) as well as the P and R rates of prokaryotic heterotrophic production (PHP), AP as well as the P and R rates of PHP, primary production (PPnet), the prokaryotic and phototrophic stocks and basic hydrological parameters were examined. Three different water masses were found, with a thermohaline front (THF) being detected between the warmer and less saline coastal waters and colder and saltier offshore Adriatic waters. Under the general oligotrophic conditions of the entire Gulf, a decreasing gradient from the coastal toward the offshore areas was detected, with PHP, PPnet, stocks and EEA (αG, ßG, AP) being directly correlated with the temperature and inversely correlated with the salinity, whereas opposite relationships were observed for LAP activity. No enhancement of microbiological activities or stocks was observed at the THF. The use of P or R rates of microbiological activities, which decrease particularly for EEA, could result in discrepancies in interpreting the efficiency of several metabolic processes.

Keywords

Offshore Area Offshore Water Prokaryotic Community Deep Chlorophyll Maximum Leucine Uptake 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors thank the captain and the crew of the R/V Urania and all the colleagues who helped in the field. The study was performed within the Cluster 10 - SAM Program Advanced Monitoring Systems funded by the Italian National Ministry for Scientific Research. Special thanks are also due to two anonymous reviewers for their substantial comments and suggestions which improved the manuscript.

References

  1. 1.
    Artegiani A, Bregant D, Paschini E, Pinardi N, Raicich F, Russo A (1997) The Adriatic Sea general circulation. Part I: air-sea interactions and water mass structure. J Phys Oceanogr 27:1492–1514. doi: 10.1175/1520-0485(1997)027<1492:TASGCP>2.0.CO;2 CrossRefGoogle Scholar
  2. 2.
    Azzaro M, La Ferla R, Maimone G, Monticelli LS, Zaccone R, Civitarese G (2012) Prokaryotic dynamics and heterotrophic metabolism in a deep convection site of Eastern Mediterranean Sea (the Southern Adriatic Pit). Cont Shelf Res 44:106–118. doi: 10.1016/j.csr.2011.07.011 CrossRefGoogle Scholar
  3. 3.
    Bianchi A, Tholosan O, Garcin J, Polychronaki T, Tselepides BR, Duinevelt G (2003) Microbial activities at the benthic boundary layer in the Aegean Sea. Progr Oceanogr 57:219–236. doi: 10.1016/S0079-6611(03)00034-X CrossRefGoogle Scholar
  4. 4.
    Bianchi CN, Zurlini G (1984) Criteri e prospettive di una classificazione ecotipologica dei sistemi marini costieri italiani. Acqua aria 8:785–796Google Scholar
  5. 5.
    Campanelli A, Cabrini M, Grilli F, Fornasaro D, Penna P, Kljajic Z, Marini M (2013) Physical, biochemical and biological characterization of two opposite areas in the Southern Adriatic Sea (Mediterranean Sea). Open J Mar Sci 3:121–131. doi: 10.4236/ojms.2013.32013 CrossRefGoogle Scholar
  6. 6.
    Caruso G (2010) Leucine aminopeptidase, beta-glucosidase and alkaline phosphatase activity rates and their significance in nutrient cycles in some coastal Mediterranean sites. Mar Drugs 8(4):916–940. doi: 10.3390/md8040916 PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Caruso G, Leonardi M, Monticelli LS, Decembrini F, Azzaro F, Crisafi E, Zappalà G, Bergamasco A, Vizzini S (2010) Assessment of the ecological status of transitional waters in Sicily (Italy): first characterization and classification according to a multiparametric approach. Mar Poll Bull 60(10):1682–1690. doi: 10.1016/j.marpolbul.2010.06.047 CrossRefGoogle Scholar
  8. 8.
    Caruso G, Caroppo C, Crisafi E, Decembrini F, Monticelli LS (2012) Struttura e attività della comunità microbica lungo il gradiente termoalino del Golfo di Manfredonia, Adriatico Centro-meridionale (Campagna SAMCA-3, maggio 2003). Biol Mar Medit 19(1):41–44Google Scholar
  9. 9.
    Caruso G, Azzaro F, La Ferla R, De Pasquale F, Raffa F, Decembrini F (2013) Microbial enzymatic activities and prokaryotic abundance in the upwelling system of the Straits of Messina (Sicily): distribution, dynamics and biogeochemical considerations. Adv Oceanogr Limnol 4(1):43–69. doi: 10.1080/19475721.2012.755568 CrossRefGoogle Scholar
  10. 10.
    Celussi M, Del Negro P (2012) Microbial degradation at a shallow coastal site: long-term spectra and rates of exoenzymatic activities in the NE Adriatic Sea. Estuar Coast Shelf Sci 115:75–86. doi: 10.1016/j.ecss.2012.02.002 CrossRefGoogle Scholar
  11. 11.
    Cho BC, Azam F (1988) Major role of bacteria in biogeochemical fluxes in the ocean's interior. Nature 332:441–443. doi: 10.1038/332441a0 CrossRefGoogle Scholar
  12. 12.
    Cho BC, Azam F (1990) Biogeochemical significance of bacterial biomass in the ocean’s euphotic zone. Mar Ecol Prog Ser 63:253–259CrossRefGoogle Scholar
  13. 13.
    Cochrane SKJ, Connor DW, Nilsson P, Mitchell I, Reker J, Franco J, Valavanis V, Moncheva S, Ekebom J, Nygaard K, Serrao Santos R, Naberhaus I, Packeiser T, Van de Bund W, Cardoso AC (2010) Marine strategy framework guidance on the interpretation and application of descriptor 1: biological diversity. Report by Task Group 1 on Biological diversity for the European Commission's Joint Research. Ispra, Italy, pp 1–114Google Scholar
  14. 14.
    Cole JJ, Likens GE, Strayer DL (1982) Photosynthetically produced dissolved organic carbon: an important carbon source for planktonic bacteria. Limnol Oceanogr 27:1080–1090. doi: 10.4319/lo.1982.27.6.1080 CrossRefGoogle Scholar
  15. 15.
    Corinaldesi C, Crevatin E, Del Negro P, Marini M, Russo A, Fonda Umani S, Danovaro R (2003) Large-scale spatial distribution of virioplankton in the Adriatic Sea: testing the trophic state control hypothesis. Appl Environ Microbiol 69:2664–2673. doi: 10.1128/AEM.69.5.2664-2673.2003 PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Cossarini G, Solidoro C, Fonda Umani S (2012) Dynamics of biogeochemical properties in temperate coastal areas of freshwater influence: lessons from the Northern Adriatic Sea (Gulf of Trieste). Estuar Coast Shelf Sci 115:63–74. doi: 10.1016/j.ecss.2012.02.006 CrossRefGoogle Scholar
  17. 17.
    Cunha MA, Almeira MA, Alcántara F (2000) Patterns of ectoenzymatic and heterotrophic bacterial activities along a salinity gradient in a shallow tidal estuary. Mar Ecol Prog Ser 204:1–12. doi: 10.3354/meps204001 CrossRefGoogle Scholar
  18. 18.
    Daims H, Wagner M (2007) Quantification of uncultured microorganisms by fluorescence microscopy and digital image analysis. Appl Microbiol Biotechnol 75:237–248. doi: 10.1007/s00253-007-0886-z PubMedCrossRefGoogle Scholar
  19. 19.
    Damiani V, Bianchi CN, Ferretti O, Bedulli D, Morri C, Viel M, Zurlini G (1988) Risultati di una ricerca ecologica sul sistema marino pugliese. Thalassia Salentina 18:153–169Google Scholar
  20. 20.
    Danovaro R, Marrale D, Della Croce N, Dell' Anno A, Fabiano M (1998) Heterotrophic nanoflagellates, bacteria and labile organic compounds in continental shelf and deep sea sediments of eastern Mediterranean. Microb Ecol 35:244–255. doi: 10.1007/s002489900080 PubMedCrossRefGoogle Scholar
  21. 21.
    Degobbis D (1990) A stoichiometric model of nutrient cycling in the Northern Adriatic Sea and its relation to regeneration processes. Mar Chem 29:235–253CrossRefGoogle Scholar
  22. 22.
    Del Giorgio PA, Condon R, Bouvier T, Longnecker K, Bouvier C, Sherr E, Gasol JM (2011) Coherent patterns in bacterial growth, growth efficiency, and leucine metabolism along a northeastern Pacific inshore–offshore transect. Limnol Oceanogr 56(1):1–16. doi: 10.4319/lo.2011.56.1.0001 CrossRefGoogle Scholar
  23. 23.
    Ducklow H (2000) Bacterial production and biomass in the oceans. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, New York, pp 85–120Google Scholar
  24. 24.
    Ducklow HW, Carlson CC (1992) Oceanic bacterial production. In: Marshall KC (ed) Advances in microbial ecology. Plenum Press, New York, pp 113–181CrossRefGoogle Scholar
  25. 25.
    Ducklow HW, Kirchman DL, Anderson TR (2002) The magnitude of spring bacterial production in the North Atlantic Ocean. Limnol Oceanogr 7:1684–1693. doi: 10.4319/lo.2002.47.6.1684 CrossRefGoogle Scholar
  26. 26.
    EC, European Commission Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for Community action in the field of marine environmental policy (Marine Strategy Framework Directive). Official Journal of the European Community, 2008, Brussels L164Google Scholar
  27. 27.
    Fagerbakke KM, Heldal M, Norland S (1996) Content of carbon, nitrogen, sulphur and phosphorus in native and cultured bacteria. Aquat Microb Ecol 10:15–27. doi: 10.3354/ame010015 CrossRefGoogle Scholar
  28. 28.
    Fernández M, Bianchi M, Van Wambeke F (1994) Bacterial biomass, heterotrophic production and utilization of dissolved organic matter photosynthetically produced in the Almeria–Oran front. J Mar Syst 5:313–325. doi: 10.1016/0924-7963(94)90053-1 CrossRefGoogle Scholar
  29. 29.
    Fiesoletti F, Specchiulli A, Spagnoli F, Galletta M, Raffa F, Decembrini F (2005) Caratteristiche fisico–chimiche, chimiche e biologiche delle acque nel golfo di Manfredonia (Adriatico Meridionale). Biol Mar Medit 12(1):445–449Google Scholar
  30. 30.
    Focardi S, Specchiulli A, Spagnoli F, Fiesoletti F, Rossi C (2009) A combined approach to investigate the biochemistry and hydrography of a shallow bay in the South Adriatic Sea: the Gulf of Manfredonia (Italy). Environ Monit Assess 153:209–220. doi: 10.1007/s10661-008-0350-2 PubMedCrossRefGoogle Scholar
  31. 31.
    Fonda Umani S, Malfatti F, Del Negro P (2012) Carbon fluxes in the pelagic ecosystem of the Gulf of Trieste. Estuar Coast Shelf Sci 115:170–185. doi: 10.1016/j.ecss.2012.04.006 CrossRefGoogle Scholar
  32. 32.
    Fuhrman JA, Ammerman JW, Azam F (1980) Bacterioplankton in the coastal euphotic zone: distribution, activity and possible relationships with phytoplankton. Mar Biol 60:201–207. doi: 10.1007/BF00389163 CrossRefGoogle Scholar
  33. 33.
    Fukami K, Murata N, Morio Y, Nishijima T (1996) Distribution of heterotrophic nanoflagellates and their importance as the bacterial consumer in a eutrophic coastal seawater. J Oceanogr 52:399–407. doi: 10.1007/BF02239045 CrossRefGoogle Scholar
  34. 34.
    Fukuda R, Ogawa H, Nagata T, Koike I (1998) Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl Environ Microbiol 64:3352–3358PubMedCentralPubMedGoogle Scholar
  35. 35.
    Fry JC (1988) Determination of biomass. In: Austin B (ed) Methods in aquatic bacteriology. John Wiley & Sons, New York, pp 27–72Google Scholar
  36. 36.
    Giani M, Diakovac T, Degobbis D, Cozzi S, Solidoro C, Fonda Umani S (2012) Recent changes in the marine ecosystems of the northern Adriatic Sea. Estuar Coast Shelf Sci 115:1–13. doi: 10.1016/j.ecss.2012.08.023
  37. 37.
    Goffart A, Hecq JH, Prieur L (1995) Controle du phyroplancton du bassin Ligure per le front Liguro–Provencal (sector Corse). Oceanol Acta 18(3):329–342Google Scholar
  38. 38.
    Gonzalez-Gil S, Keafer BA, Jovine RVM, Aguilera A, Lu S, Anderson DM (1998) Detection and quantification of alkaline phosphatase in single cells of phosphorus – starved marine phytoplankton. Mar Ecol Prog Ser 164:21–35. doi: 10.3354/meps164021 CrossRefGoogle Scholar
  39. 39.
    Grasshoff K (1983) Determination of nitrate. In: Grasshoff K, Ehrhardt M, Kremling K (eds) Methods of sea water analysis. Weinheim, Verlag Chemie, pp 143–150Google Scholar
  40. 40.
    Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Paleontol Electron 4(1):9Google Scholar
  41. 41.
    Hoch MP, Kirchman DL (1993) Seasonal and inter-annual variability in bacterial production and biomass in a temperate estuary. Mar Ecol Progr Ser 98:283–295. doi: 10.3354/meps098283 CrossRefGoogle Scholar
  42. 42.
    Hopkins T, Artegiani A, Kinder C and Pariente R (1998) Description of the Northern Adriatic circulation as computed from the ELNA hydrography. In: Hopkins TS Artegiani A, Cauwet G, Degobbis D, Malej A (eds) The Adriatic Sea, ecosystem research report no. 32, 1999, EUR 18834, European Commission, BrusselsGoogle Scholar
  43. 43.
    Hoppe HG (1983) Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Mar Ecol Progr Ser 11:299–308. doi: 10.3354/meps011299 CrossRefGoogle Scholar
  44. 44.
    Hoppe HG (1993) Use of fluorogenic model substrates for extracellular enzyme activity (EEA) measurement of bacteria. In: Kemp PR, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods in aquatic microbial ecology. Lewis Publishers, Boca Raton, pp 423–431Google Scholar
  45. 45.
    Hoppe HG (2003) Phosphatase activity in the sea. Hydrobiologia 493:187–200CrossRefGoogle Scholar
  46. 46.
    Hoppe HG, Arnosti C, Herndl GF (2002) Ecological significance of bacterial enzymes in the marine environment. In: Burn RG, Dick RP (eds) Enzymes in the environment: activity, ecology and applications. Marcel Dekker, New York, pp 73–107Google Scholar
  47. 47.
    Hoppe HG, Ullrich S (1999) Profiles of ectoenzymes in the Indian Ocean: phenomena of phosphatase activity in the mesopelagic zone. Aquat Microb Ecol 19:139–148. doi: 10.3354/ame019139 CrossRefGoogle Scholar
  48. 48.
    Ivancic I, Fuks D, Radic T, Lyons DM, Silovic T, Kraus R, Precali R (2010) Phytoplankton and bacterial alkaline phosphatase activity in the northern Adriatic Sea. Mar Environ Res 69:85–94. doi: 10.1016/j.marenvres.2009.08.004 PubMedCrossRefGoogle Scholar
  49. 49.
    Jacquet S, Prieur L, Avois-Jacquet C, Leennon JF, Vaulot D (2002) Short-timescale variability of picophytoplankton abundance and cellular parameters in surface waters of the Alboran Sea (western Mediterranean). J Plankton Res 24(7):635–651CrossRefGoogle Scholar
  50. 50.
    Jones RD (1997) Phosphorus cycling. In: Hurst CJ (ed) Manual of environmental microbiology. ASM Press, Washington, D.C., pp 343–348Google Scholar
  51. 51.
    Kawasaki N, Benner R (2006) Bacterial release of dissolved organic matter during cell growth and decline: molecular origin and composition. Limnol Oceanogr 51:2170–2180. doi: 10.4319/lo.2006.51.5.2170 CrossRefGoogle Scholar
  52. 52.
    Kirchman DL (1993) Leucine incorporation as a measure of biomass production by heterotrophic bacteria. In: Kemp PR, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods in aquatic microbial ecology. Lewis Publishers, Boca Raton, pp 509–512Google Scholar
  53. 53.
    Kirchman DL, Newell SY, Hodson RE (1986) Incorporation versus biosynthesis of leucine: implications for measuring rates of protein synthesis and biomass production by bacteria in marine systems. Mar Ecol Progr Ser 32:47–59. doi: 10.3354/meps032047 CrossRefGoogle Scholar
  54. 54.
    Kovacevic V, Gacic M, Poulain PM (1999) Eulerian current measurements in the Strait of Otranto and in Southern Adriatic. J Mar Syst 20:255–278. doi: 10.1016/S0924-7963(98)00086-4 CrossRefGoogle Scholar
  55. 55.
    La Ferla R, Leonardi M (2005) Ecological implications of biomass and morphotype variations of bacterioplankton: and example in a coastal zone of the Northern Adriatic Sea (Mediterranean). Mar Ecol 26:82–88. doi: 10.1111/j.1439-0485.2005.00049.x CrossRefGoogle Scholar
  56. 56.
    La Ferla R, Zaccone R, Azzaro M, Caruso G (2002) Microbial respiratory and ectoenzymatic activities in the Northern Adriatic Sea (Mediterranean Sea). Chem Ecol 18:75–84. doi: 10.1080/02757540212693 CrossRefGoogle Scholar
  57. 57.
    Lee S, Fuhrman JE (1987) Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl Environ Microbiol 53:1298–1303PubMedCentralPubMedGoogle Scholar
  58. 58.
    Lee CW, Bong CW, Hii YS (2009) Temporal variation of bacterial respiration and growth efficiency in tropical coastal waters. Appl Environ Microbiol 75(24):7594–7601. doi: 10.1128/AEM.01227-09 PubMedCentralPubMedCrossRefGoogle Scholar
  59. 59.
    Li H, Veldhuis MJW, Post AF (1998) Alkaline phosphatase activities among planktonic communities in the northern Red Sea. Mar Ecol Progr Ser 173:107–115. doi: 10.3354/meps173107 CrossRefGoogle Scholar
  60. 60.
    Long RA, Azam F (1996) Abundant protein-containing particles in the sea. Aquat Microb Ecol 10:213–221. doi: 10.3354/ame010213 CrossRefGoogle Scholar
  61. 61.
    Lonborg C, Martinez-Garcia S, Teira E, Alvarez-Salgado XA (2011) Bacterial carbon demand and growth efficiency in a coastal upwelling system. Aquat Microb Ecol 96:183–191. doi: 10.3354/ame01495 CrossRefGoogle Scholar
  62. 62.
    Lorenzen CI (1967) Determination of chlorophyll and pheopigments: spectrophotometric equations. Limnol Oceanogr 12:343–346. doi: 10.4319/lo.1967.12.2.0343 CrossRefGoogle Scholar
  63. 63.
    Mahowald N, Jickells TD, Baker AR, Artaxo P, Benitez-Nelson CR, Bergametti G, Bond TC, Chen Y, Cohen DD, Herut B, Kubilay N, Losno R, Luo C, Maenhaut W, McGee KA, Okin GS, Siefert RL, Tsukuda S (2008) Global distribution of atmospheric phosphorus sources, concentrations and deposition rates, and anthropogenic impacts. Global Biogeochem Cycles 22, GB4026. doi: 10.1029/2008GB003240 CrossRefGoogle Scholar
  64. 64.
    Manca B, Franco P, Paschini E (2001) Seasonal variability of the hydrography in the Adriatic Sea: water mass properties and circulation. In: Faranda FM, Guglielmo L, Spezie G (eds) Mediterranean ecosystems: structures and processes. Springer Verlag, Italy, pp 45–60CrossRefGoogle Scholar
  65. 65.
    Mann KH, Lazier JRN (1996) Dynamics of marine ecosystems. Biological–physical interactions in the oceans, 2nd ed. Blackwell Science, CambridgeGoogle Scholar
  66. 66.
    Mazzoleni LR, Ehrmann BM, Shen X, Marshall AG, Collett JL Jr (2010) Water soluble atmospheric organic matter in fog: exact masses and chemical formula identification by ultrahigh resolution Fourier transform ion cyclotron resonance mass spectrometry. Environ Sci Technol 44:3690–3697. doi: 10.1021/es903409k PubMedCrossRefGoogle Scholar
  67. 67.
    Middelboe M, Sǿndergaard M, Letarte Y, Borch NH (1995) Attached and free-living bacteria: production and polymer hydrolysis during a diatom bloom. Microb Ecol 29:231–248. doi: 10.1007/BF00164887 PubMedCrossRefGoogle Scholar
  68. 68.
    Misic C, Fabiano M (2006) Ectoenzymatic activity and its relationship to chlorophyll-a and bacteria in the Gulf of Genoa (Ligurian Sea, NW Mediterranean). J Mar Syst 60:193–206. doi: 10.1016/j.jmarsys.2005.10.006 CrossRefGoogle Scholar
  69. 69.
    Molari M, Giovannelli D, D'Errico G, Manini E (2012) Factors influencing prokaryotic community structure composition in sub-surface coastal sediments. Estuar Coast Shelf Sci 97:141–148. doi: 10.1016/j.ecss.2011.11.036 CrossRefGoogle Scholar
  70. 70.
    Moran XAG, Taupier-Letage I, Vázquez-Domínguez E, Ruiz S, Arin L, Raimbault P, Estrada M (2001) Physical–biological coupling in the Algerian Basin (SW Mediterranean): influence of mesoscale instabilities in the biomass and production of phytoplankton and bacterioplankton. Deep Sea Res I 48:405–437. doi: 10.1016/S0967-0637(00)00042-X CrossRefGoogle Scholar
  71. 71.
    Naganuma T (1997) Abundance and production of bacterioplankton along a transect of Ise Bay, Japan. J Oceanogr 53:579–583Google Scholar
  72. 72.
    Pasaric Z, Belusic D, Klaic ZB (2007) Orographic influence on the Adriatic sirocco wind. Ann Geophys 25:1263–1267. doi: 10.5194/angeo-25-1263-2007 CrossRefGoogle Scholar
  73. 73.
    Pettine M, Patrolecco L, Camusso M, Crescenzio S (1998) Transport of carbon and nitrogen to the northern Adriatic sea by the Po river. Estuar Coast Shelf Sci 46:127–142. doi: 10.1006/ecss.1997.0303 CrossRefGoogle Scholar
  74. 74.
    Pollard PC, Moriarty DJW (1984) Validity of the tritiated thymidine methods for estimating bacterial growth rates: measurement of isotope dilution during DNA synthesis. Appl Environ Microbiol 48(6):1076–1083PubMedCentralPubMedGoogle Scholar
  75. 75.
    Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948. doi: 10.4319/lo.1980.25.5.0943 CrossRefGoogle Scholar
  76. 76.
    Pusceddu A, Dell’Anno A, Vezzulli L, Fabiano M, Saggiomo V, Cozzi S, Catalano G, Guglielmo L (2009) Microbial loop malfunctioning in the annual sea ice at Terra Nova Bay (Antarctica). Polar Biol 32:337–346. doi: 10.1007/s00300-0080539-4 CrossRefGoogle Scholar
  77. 77.
    Poulain PM (1999) Drifter observations of surface circulation in the Adriatic Sea between December 1994 and March 1996. J Mar Syst 20:231–253. doi: 10.1016/S0924-7963(98)00084-0 CrossRefGoogle Scholar
  78. 78.
    Poulain PM (2001) Adriatic Sea surface circulation as derived from drifter between 1990 and 1999. J Mar Syst 29:3–32. doi: 10.1016/S0924-7963(01)00007-0 CrossRefGoogle Scholar
  79. 79.
    Puddu A, La Ferla R, Allegra A, Bacci C, Lopez M, Oliva F, Pierotti C (1998) Seasonal and spatial distribution of bacterial production and biomass along a salinity gradient (Northern Adriatic Sea). Hydrobiologia 363:271–282. doi: 10.1023/A:1003169620843 CrossRefGoogle Scholar
  80. 80.
    Puddu A, Alberighi L, Del Negro P, Manganelli M, Zaccone R (2000) Cicli giornalieri di produzione e abbondanza microbiche in acque costiere superficiali del Nord Adriatico. Biol Mar Medit 7:196–205Google Scholar
  81. 81.
    Pugnetti A, Armeni M, Camatti E, Crevatin E, Dell’Anno A, Del Negro P, Milandri A, Socal G, Fonda Umani S, Danovaro R (2005) Imbalance between phytoplankton production and bacterial carbon demand in relation to mucilage formation in the Northern Adriatic Sea. Sci Total Environ 353:162–177. doi: 10.1016/j.scitotenv.2005.09.014 PubMedCrossRefGoogle Scholar
  82. 82.
    Rabouille C, Mackenzie FT, Ver LM (2001) Influence of the human perturbation on carbon, nitrogen, and oxygen biogeochemical cycles in the global coastal ocean. Geochim Cosmochim Acta 65(21):3615–3641. doi: 10.1016/S0016-7037(01)00760-8 CrossRefGoogle Scholar
  83. 83.
    Rath J, Schiller C, Herndl GJ (1993) Ectoenzymatic activity and bacterial dynamics along a trophic gradient in the Caribbean Sea. Mar Ecol Prog Ser 102:89–96CrossRefGoogle Scholar
  84. 84.
    Raffa F, Decembrini F, Hopkins TS (2008) Hydrophysical mesoscale factors affecting phytoplankton distribution in a southern Adriatic Sea coastal area (Gulf of Manfredonia). In: Proceedings of the Italian Association of Oceanology and Limnology, Pallianza, Italy, pp. 405–410Google Scholar
  85. 85.
    Samo TJ, Pedler BE, Ball GI, Pasulka AL, Taylor AG, Aluwihare LI, Azam F, Goericke R, Landry MR (2012) Microbial distribution and activity across a water mass frontal zone in the California Current Ecosystem. J Plank Res 34(9):802–814. doi: 10.1093/plankt/fbs048 CrossRefGoogle Scholar
  86. 86.
    Sebastián M, Arístegui J, Montero MF, Xavier Niell F (2004) Kinetics of alkaline phosphatase activity, and effect of phosphate enrichment: a case study in the NW African upwelling region. Mar Ecol Progr Ser 270:1–13. doi: 10.3354/meps270001 CrossRefGoogle Scholar
  87. 87.
    Sieracki ME, Viles CL, Webb KL (1989) Algorithm to estimate cell biovolume using image analyzed microscopy. Cytometry 10:551–557. doi: 10.1002/cyto.990100510 PubMedCrossRefGoogle Scholar
  88. 88.
    Siuda W, Kiersztyn B, Chrost RJ (2007) The dynamics of protein decomposition in lakes of different trophic status – reflections on the assessment of the real proteolytic activity in situ. J Microbiol Biotechnol 17(6):897–904PubMedGoogle Scholar
  89. 89.
    Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs 6:107–114Google Scholar
  90. 90.
    Smith DC, Simon M, Alldredge AL, Azam F (1992) Intense hydrolytic enzyme activity on marine aggregates and implication for rapid particle dissolution. Nature 359:139–142. doi: 10.1038/359139a0 CrossRefGoogle Scholar
  91. 91.
    Spagnoli F, Bartholini G, Marini M, Giordano P (2004) Biogeochemical processes in sediments of the Manfredonia Gulf (Southern Adriatic Sea): early diagenesis of carbon and nutrients and benthic exchange. Biogeosci Disc 1:803–824. doi: 10.5194/bgd-1-803-2004 CrossRefGoogle Scholar
  92. 92.
    Spagnoli F, Dell’Anno A, De Marco A, Dinelli E, Fabiano M, Gadaleta MV, Ianni C, Loiacono F, Manini E, Marini M, Mongelli G, Rampazzo G, Rivaro P, Vezzulli L (2010) Biogeochemistry, grain size and mineralogy of the central and southern Adriatic Sea sediments: a review. Chem Ecol 26(Suppl):19–44. doi: 10.1080/02757541003689829 CrossRefGoogle Scholar
  93. 93.
    Steeman-Nielsen E (1952) The use of radioactive carbon (C14) for measuring organic production in the sea. ICES J Mar Sci 18(2):117–140. doi: 10.1093/icesjms/18.2.117 CrossRefGoogle Scholar
  94. 94.
    Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Bulletin 167, 2nd edition. Fisher Res Bd Canada, Ottawa, pp 1–311Google Scholar
  95. 95.
    Strom SL, Benner R, Ziegler S, Dago MJ (1997) Planktonic grazers are a potential important source of marine dissolved organic carbon. Limnol Oceanogr 42:1364–1374CrossRefGoogle Scholar
  96. 96.
    Suzumura M, Hashihama F, Yamada N, Kinouchi S (2012) Dissolved phosphorus pools and alkaline phosphatase activity in the euphotic zone of the western North Pacific Ocean. Front Microbiol 3:99. doi: 10.3389/fmicb.2012.00099 PubMedCentralPubMedCrossRefGoogle Scholar
  97. 97.
    Tamburini C, Garcin J, Ragot M, Bianchi A (2002) Biopolymer hydrolysis and bacterial production under ambient hydrostatic pressure though a 2000 m water column in the NW Mediterranean. Deep Sea Res II 49:2109–2123. doi: 10.1016/S0967-0645(02)00030-9 CrossRefGoogle Scholar
  98. 98.
    Unanue M, Ayo B, Azua I, Barcina J, Iriberri J (1992) Temporal variability of attached and free-living bacteria in coastal waters. Microb Ecol 23:27–39. doi: 10.1007/BF00165905 PubMedCrossRefGoogle Scholar
  99. 99.
    Van Wambeke F, Christake U, Giannakourou A, Moutin T, Souvemerzoglou K (2002) Longitudinal and vertical trends of bacterial limitation by phosphorus and carbon in the Mediterranean Sea. Microb Ecol 43:119–133. doi: 10.1007/s00248-001-0038-4 PubMedCrossRefGoogle Scholar
  100. 100.
    Van Wambeke F, Heussner S, Diaz F, Raimbault P, Conaan P (2002) Small-scale variability in the coupling/uncoupling of bacteria, phytoplankton and organic carbon fluxes along the continental margin of the Gulf of Lions, Northwestern Mediterranean Sea. J Mar Syst 33–34:411–429. doi: 10.1016/S0924-7963(02)00069-6 CrossRefGoogle Scholar
  101. 101.
    Van Wambeke F, Lefèvre D, Prieur L, Sempéré R, Bianchi M, Oubelkheir K, Bruyant F (2004) Distribution of microbial biomass, production, respiration, dissolved organic carbon and factors controlling bacterial production across a geostrophic front (Almeria–Oran, SW Mediterranean Sea). Mar Ecol Progr Ser 269:1–15. doi: 10.3354/meps269001 CrossRefGoogle Scholar
  102. 102.
    Vilicic D, Vucak Z, Skrivanic A, Grzetic Z (1989) Phytoplankton blooms in the oligotrophic open South Adriatic waters. Mar Chem 28:89–107. doi: 10.1016/0304-4203(89)90189-8 CrossRefGoogle Scholar
  103. 103.
    Villarreal-Chiu JF, Quinn JP, McGrath JW (2012) The genes and enzymes of phosphonate metabolism by bacteria, and their distribution in the marine environment. Front Microbiol 3:19. doi: 10.3389/fmicb.2012.00019 PubMedCentralPubMedCrossRefGoogle Scholar
  104. 104.
    Wallenstein MD, Weintraub MN (2008) Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biol Biochem 40:2098–2106. doi: 10.1016/j.soilbio.2008.01.024 CrossRefGoogle Scholar
  105. 105.
    White A, Dyhrman S (2013) The marine phosphorus cycle. Front Microbiol 4:105. doi: 10.3389/fmicb.2013.00105 PubMedCentralPubMedCrossRefGoogle Scholar
  106. 106.
    Wilhelm SW, Brigden SM, Suttle CA (2003) A dilution technique for the measurement of viral production: a comparison in stratified and tidal mixed coastal waters. Microb Ecol 43:168–173. doi: 10.1007/s00248-001-1021-9 CrossRefGoogle Scholar
  107. 107.
    Willey JD, Kieber RJ, Eyman MS, Brooks Avery Jr C (2000) Rainwater dissolved organic carbon: concentrations and global flux. Global Biogeochem Cycles 14(1):139–148. doi: 10.1029/1999GB900036 CrossRefGoogle Scholar
  108. 108.
    Yanagi T, Guo X, Saino T, Ishimaru T, Noriki S (1997) Thermohaline front at the Mouth of Ise Bay. J Oceanogr 53:403–409Google Scholar
  109. 109.
    Yentsch CS, Menzel DW (1963) A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep Sea Res 7:221–231. doi: 10.1016/0011-7471(63)90358-9 Google Scholar
  110. 110.
    Yuasa I, Hashimoto E, Ueshima H (1993) Nitrogen and phosphorus distribution across the thermohaline front in Kii Channel in winter. J Oceanogr 49:407–424CrossRefGoogle Scholar
  111. 111.
    Zaccone R, Caruso G (2002) Microbial hydrolysis of polysaccharides and organic phosphates in the Northern Adriatic sea. Chem Ecol 18:85–94. doi: 10.1080/02757540212691 CrossRefGoogle Scholar
  112. 112.
    Zaccone R, Monticelli LS, Seritti A, Santinelli C, Azzaro M, Boldrin A, La Ferla R, Ribera d'Alcalà M (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. J Geophys Res 108(C9):8117. doi: 10.1029/2002JC001625 CrossRefGoogle Scholar
  113. 113.
    Zaccone R, Boldrin A, Caruso G, La Ferla R, Maimone G, Santinelli C, Turchetto M (2012) Enzymatic activities and prokaryotic abundance in relation to organic matter along a West–East Mediterranean Transect (TRANSMED Cruise). Microb Ecol 64:54–66PubMedCrossRefGoogle Scholar
  114. 114.
    Zavatarelli M, Baretta JG, Baretta-Bekker JG, Pinardi N (2000) The dynamics of the Adriatic ecosystem; an idealized model study. Deep Sea Res 47:937–970CrossRefGoogle Scholar
  115. 115.
    Zavatarelli M, Raicich F, Bregant D, Russo A, Artegiani A (1998) Climatological biogeochemical characteristics of the Adriatic Sea. J Mar Syst 18:227–263. doi: 10.1016/S0924-7963(98)00014-1 CrossRefGoogle Scholar
  116. 116.
    Zoppini A, Puddu A, Fazi S, Rosati M, Sist P (2005) Extracellular enzyme activity and dynamics of bacterial community in mucilaginous aggregates of the northern Adriatic Sea. Sci Total Environ 353:270–286. doi: 10.1016/j.scitotenv.2005.09.019 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • L. S. Monticelli
    • 1
    Email author
  • G. Caruso
    • 1
  • F. Decembrini
    • 1
  • C. Caroppo
    • 2
  • F. Fiesoletti
    • 3
  1. 1.CNR-Institute for Coastal Marine Environment: Section of MessinaMessinaItaly
  2. 2.CNR-Institute for Coastal Marine Environment: Section of TarantoTarantoItaly
  3. 3.CNR-ISMAR Section of LesinaLesinaItaly

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