Skip to main content

Advertisement

SpringerLink
Log in

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)

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

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.

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

Similar content being viewed by others

References

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  4. Bianchi CN, Zurlini G (1984) Criteri e prospettive di una classificazione ecotipologica dei sistemi marini costieri italiani. Acqua aria 8:785–796

    Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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):41–44

    Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  12. Cho BC, Azam F (1990) Biogeochemical significance of bacterial biomass in the ocean’s euphotic zone. Mar Ecol Prog Ser 63:253–259

    Article  CAS  Google Scholar 

  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 1–114

  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

    Article  CAS  Google Scholar 

  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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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 18:153–169

    Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  21. Degobbis D (1990) A stoichiometric model of nutrient cycling in the Northern Adriatic Sea and its relation to regeneration processes. Mar Chem 29:235–253

    Article  CAS  Google Scholar 

  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

    Article  Google Scholar 

  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 85–120

    Google Scholar 

  24. Ducklow HW, Carlson CC (1992) Oceanic bacterial production. In: Marshall KC (ed) Advances in microbial ecology. Plenum Press, New York, pp 113–181

    Chapter  Google Scholar 

  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

    Article  Google Scholar 

  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 L164

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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):445–449

    Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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 64:3352–3358

    PubMed Central  CAS  PubMed  Google Scholar 

  35. Fry JC (1988) Determination of biomass. In: Austin B (ed) Methods in aquatic bacteriology. John Wiley & Sons, New York, pp 27–72

  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. Goffart A, Hecq JH, Prieur L (1995) Controle du phyroplancton du bassin Ligure per le front Liguro–Provencal (sector Corse). Oceanol Acta 18(3):329–342

    Google Scholar 

  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

    Article  CAS  Google Scholar 

  39. Grasshoff K (1983) Determination of nitrate. In: Grasshoff K, Ehrhardt M, Kremling K (eds) Methods of sea water analysis. Weinheim, Verlag Chemie, pp 143–150

    Google Scholar 

  40. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Paleontol Electron 4(1):9

    Google Scholar 

  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

    Article  Google Scholar 

  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, Brussels

  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

    Article  CAS  Google Scholar 

  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 423–431

    Google Scholar 

  45. Hoppe HG (2003) Phosphatase activity in the sea. Hydrobiologia 493:187–200

    Article  CAS  Google Scholar 

  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 73–107

    Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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):635–651

    Article  CAS  Google Scholar 

  50. Jones RD (1997) Phosphorus cycling. In: Hurst CJ (ed) Manual of environmental microbiology. ASM Press, Washington, D.C., pp 343–348

    Google Scholar 

  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

    Article  CAS  Google Scholar 

  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 509–512

    Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  57. Lee S, Fuhrman JE (1987) Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl Environ Microbiol 53:1298–1303

    PubMed Central  CAS  PubMed  Google Scholar 

  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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  60. Long RA, Azam F (1996) Abundant protein-containing particles in the sea. Aquat Microb Ecol 10:213–221. doi:10.3354/ame010213

    Article  Google Scholar 

  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

    Article  Google Scholar 

  62. Lorenzen CI (1967) Determination of chlorophyll and pheopigments: spectrophotometric equations. Limnol Oceanogr 12:343–346. doi:10.4319/lo.1967.12.2.0343

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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 45–60

    Chapter  Google Scholar 

  65. Mann KH, Lazier JRN (1996) Dynamics of marine ecosystems. Biological–physical interactions in the oceans, 2nd ed. Blackwell Science, Cambridge

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  Google Scholar 

  71. Naganuma T (1997) Abundance and production of bacterioplankton along a transect of Ise Bay, Japan. J Oceanogr 53:579–583

    Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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):1076–1083

    PubMed Central  CAS  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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 7:196–205

    Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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 102:89–96

    Article  CAS  Google Scholar 

  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. 405–410

  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

    Article  CAS  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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):897–904

    CAS  PubMed  Google Scholar 

  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 6:107–114

    Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  94. Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Bulletin 167, 2nd edition. Fisher Res Bd Canada, Ottawa, pp 1–311

  95. Strom SL, Benner R, Ziegler S, Dago MJ (1997) Planktonic grazers are a potential important source of marine dissolved organic carbon. Limnol Oceanogr 42:1364–1374

    Article  CAS  Google Scholar 

  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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  105. White A, Dyhrman S (2013) The marine phosphorus cycle. Front Microbiol 4:105. doi:10.3389/fmicb.2013.00105

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  108. Yanagi T, Guo X, Saino T, Ishimaru T, Noriki S (1997) Thermohaline front at the Mouth of Ise Bay. J Oceanogr 53:403–409

    Google Scholar 

  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. Yuasa I, Hashimoto E, Ueshima H (1993) Nitrogen and phosphorus distribution across the thermohaline front in Kii Channel in winter. J Oceanogr 49:407–424

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  Google Scholar 

  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 64:54–66

    Article  CAS  PubMed  Google Scholar 

  114. Zavatarelli M, Baretta JG, Baretta-Bekker JG, Pinardi N (2000) The dynamics of the Adriatic ecosystem; an idealized model study. Deep Sea Res 47:937–970

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. CNR-Institute for Coastal Marine Environment: Section of Messina, Sp. S. Raineri, 86, 98122, Messina, Italy

    L. S. Monticelli, G. Caruso & F. Decembrini

  2. CNR-Institute for Coastal Marine Environment: Section of Taranto, via Roma, 3, 74100, Taranto, Italy

    C. Caroppo

  3. CNR-ISMAR Section of Lesina, via Pola, 4, 71010, Lesina, Italy

    F. Fiesoletti

Authors
  1. L. S. Monticelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Caruso
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. Decembrini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Caroppo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. F. Fiesoletti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. S. Monticelli.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Monticelli, L.S., Caruso, G., Decembrini, F. et al. 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). Microb Ecol 67, 501–519 (2014). https://doi.org/10.1007/s00248-013-0350-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-013-0350-9

Keywords

Search

Navigation