Composition and function of mucilage macroaggregates in the northern Adriatic

Aquatic Microbial Ecology

Volumn 61, Issue 3, 2010, Pages 279-289

  Turk, Valentina ^a   Hagström, Åke ^b   Kovač, Nives ^a   Faganeli, Jadran ^a  

^a NATIONAL INSTITUTE OF BIOLOGY   (Slovenia)

^b LINNAEUS UNIVERSITY   (Sweden)

Author keywords

Composition; Degradation; Macroaggregates; Microorganisms; Northern Adriatic

Indexed keywords

BACTERIA (MICROORGANISMS);

EID: 78650869963     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame01447     Document Type: Review

References (85)

1. Azam F, Fonda Umani S, Funari E (1999) Significance of bacteria in the mucilage phenomenon in the northern Adriatic Sea. Ann Ist Super Sanit 35:411-419
2. Baldi F, Minacci A, Saliot A, Mejanelle L, Mozetic P, Turk V, Malej A (1997) Cell lysis and release of particulate polysaccharides in extensive marine mucilage assessed by lipid biomarkers and molecular probes. Mar. Ecol Prog Ser 153:45-57
3. Benner R (2002) Chemical composition and reactivity. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Elsevier, Amsterdam, p 367-404
4. Binkley ER, Binkley RW (1999) Carbohydrate photochemistry. American Chemical Society, Washington, DC
5. Chin WC, Orellana MV, Verdugo P (1998) Spontaneous assembly of marine dissolved organic matter in polymer gels. Nature 391:568-572
6. Clark AH, Farrer DB (1995) Kinetics of biopolymer gelation - implications of a cascade theory description for the concentration, molecular weight, and temperature dependences of the shear modulus and gel time. J Rheol 39:1429-1444
7. Conan P, Sondergaard M, Kragh T, Thingstad F and others (2007) Partitioning of organic production in marine plankton communities: the effects of inorganic nutrient ratios and community composition on new dissolved organic matter. Limnol Oceanogr 52:753-765
8. Cozzi S, Ivančić I, Catalano G, Djakovac T, Degobbis D (2004) Dynamics of the oceanographic properties during mucilage appearance in the Northern Adriatic Sea: analysis of the 1997 event in comparison to earlier events. J Mar. Syst 50:223-241
9. Dalton HM, Goodman AE, Marchall KC (1996) Diversity in surface colonization behavior in marine bacteria. J Ind Microbiol Biotechnol 17:228-234
10. Danovaro R, Armeni M, Luna GM, Corinaldesi C and others (2005) Exo-enzymatic activities and dissolved organic pools in relation with mucilage development in the Northern Adriatic Sea. Sci Total Environ 353:189-203
11. Davey ME, O'Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847-867
12. Degobbis D, Precali R, Ferrari CR, Djakovac T and others (2005) Changes in nutrient concentrations and ratios during mucilage events in the period 1999-2002. Sci Total Environ 353:103-114
13. del Giorgio PA, Cole JJ (2000) Bacterial energetics and growth efficiency. In: Kirchman D (ed) Microbial ecology of the oceans. Wiley-Liss, New York, NY, p 289-325
14. Del Negro P, Crevatin E, Larato C, Ferrari C and others (2005) Mucilage microcosms. Sci Total Environ 353:258-269
15. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350-356
16. Faganeli J, Kovač N, Leskovšek H, Pezdič J (1995) Sources and fluxes of particulate organic matter in shallow coastal waters characterized by summer macroaggregate formation. Biogeochemistry 29:71-88
17. Faganeli J, Ogrinc N, Kovač N, Kukovec K, Falnoga I, Mozetič P, Bajt O (2009) Carbon and nitrogen isotope composition of particulate organic matter in relation to mucilage formation in the northern Adriatic Sea. Mar. Chem 114:102-109
18. Fajon C, Cauwet G, Lebaron P, Terzić S and others (1999) The accumulation and release of polysaccharides by planktonic cells and the subsequent bacterial response during a controlled experiment. FEMS Microbiol Ecol 29:351-363
19. Flander-Putrle V, Malej A (2008) The evolution and phytoplankton composition of mucilaginous aggregates in the northern Adriatic Sea. Harmful Algae 7:752-761
20. Fonda-Umani S, Ghirardelli E, Specchi M (1989) Gli episodi di 'mare sporco' nellAdriatico dal 1729 ai nostri giorni. Regione autonoma Friuli - Venezia Giulia, Direzione regionale dell'ambiente, Trieste
21. Fonda Umani S, Del Negro P, Larato C, De Vittor C and others (2007) Major inter-annual variations in microbial dynamics in the Gulf of Trieste (northern Adriatic Sea) and their ecosystem implications. Aquat Microb Ecol 46:163-175
22. Giani M, Degobbis D, Rinaldi A (2005a) Mucilages in the Adriatic and Tyrrhenian Seas. Sci Total Environ 353:1-2
23. Giani M, Berto D, Zangrando V, Castelli S, Sist P, Urbani R (2005b) Chemical characterization of different typologies of mucilaginous aggregates in the Northern Adriatic Sea. Sci Total Environ 353:232-246 (Pubitemid 41757614)
24. Gram L, Grossart HP, Schlingloff A, Kiørboe T (2002) Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Appl Environ Microbiol 68:4111-4116
25. Granéli E, Carlsson P, Turner JT, Tester PA, Béchemin C, Dawson R, Funari E (1999) Effects of N:P:Si ratios and zooplankton grazing on phytoplankton communities in the northern Adriatic Sea. I. Nutrients, phytoplankton biomass, and polysaccharide production. Aquat Microb Ecol 18:37-54
26. Grossart HP, Ploug H (2001) Microbial degradation of organic carbon and nitrogen on diatom aggregates. Limnol Oceanogr 46:267-277
27. Guenet JM (1992) Thermoreversible gelation of polymers and biopolymers. Academic Press, London
28. Guo L, Santschi PH (2007) Ultrafiltration and its applications to sampling and characterisation of aquatic colloids. In: Wilkinson KJ, Lead JR (eds) Environmental colloids and particles. Wiley, Chichester, p 160-221
29. Hedges JI, Stern JH (1984) Carbon and nitrogen determinations in carbonate-containing solids. Limnol Oceanogr 29:657-663
30. Heissenberger A, Leppard GC, Herndl GJ (1996) Ultrastructure of marine snow. II. Microbiological considerations. Mar. Ecol Prog Ser 135:299-308
31. Herndl GJ, Arietta JM, Stoderegger K (1999) Interaction between specific hydrological and microbial activity leading to extensive mucilage formation in the northern Adriatic Sea. Ann Ist Super Sanit 35:405-409
32. Kaltenböck E, Herndl GJ (1992) Ecology of amorphous aggregations (marine snow) in the Northern Adriatic Sea. IV. Dissolved nutrients and the autotrophic community associated with marine snow. Mar. Ecol Prog Ser 87:147-159
33. Kovač N, Faganeli J, Sket B, Bajt O (1998) Characterization of macroaggregates and photodegradation of their water soluble fraction. Org Geochem 29:1623-1634
34. 1H NMR spectroscopy. Mar. Chem 78:205-215
35. Kovač N, Faganeli J, Bajt O, Sket B, Orel B, Penna N (2004) Chemical composition of macroaggregates in the northern Adriatic. Org Geochem 35:1095-1104
36. Kovač N, Mozetič P, Trichet J, Défarge C (2005) Phytoplankton composition and organic matter organization of mucous aggregates by means of light and cryo-scanning electron microscopy. Mar. Biol 147:261-271
37. Kovač N, Faganeli J, Bajt O (2008) Mucous macroaggregates in the Northern Adriatic. In: Stefansson O (ed) Geochemistry Research Advances. Nova, New York, NY, p 119-141
38. La Ferla R, Leonardi M (2005) Ecological implications of biomass and morphotype variations of bacterioplankton: an example in the coastal zone of the northern Adriatic Sea (Mediterranean). PSZN I: Mar. Ecol 26:82-88
39. Legras JI, Chuzel G, Arnaud A, Galzy P (1990) Natural nitriles and their metabolism. World J Microbiol Biotechnol 6:83-108
40. Leppard GG, Heissenberger A, Herndl GJ (1996) Ultrastructure of marine snow. I. Transmission electron microscopy methodology. Mar. Ecol Prog Ser 135:289-298
41. Løvdal T, Skjoldal EF, Heldal M, Norland S, Thingstad TF (2008) Changes in morphology and elemental composition of Vibrio splendidus along a gradient from carbon-limited to phosphate-limited growth. Microb Ecol 55:152-161
42. Macko SA, Estep MLF, Engel MH, Hare PE (1986) Kinetic fractionation of stable nitrogen isotopes during amino acid transamination. Geochim Cosmochim Acta 50:2143-2146
43. Malej A, Harris RP (1993) Inhibition of copepod grazing by diatom exudates: a factor in the development of mucus aggregates? Mar. Ecol Prog Ser 96:33-42
44. Malej A, Petelin B, Cermelj B (2001) Quantification of mucilage-associated suspended matter in the Gulf of Trieste (Adriatic Sea). Ann Ser Hist Nat 11:43-52
45. Malej A, Mozetič P, Turk V, Terzic S, Ahel M, Cauwet G (2003) Changes in particulate and dissolved organic matter in nutrient-enriched enclosures from an area influenced by mucilage: the northern Adriatic Sea. J Plankton Res 25:949-966
46. Malfatti F, Azam F (2009) Atomic force microscopy reveals microscale networks and possible symbioses among pelagic marine bacteria. Aquat Microb Ecol 58:1-14
47. Manganelli M, Funari E (2003) Le mucillagini nel Mar. Adriatico: ruolo dei possibili agenti causali e dei fattori ambientali. Ann Ist Super Sanit 39:77-95
48. Mingazzini M, Take B (1995) Summary and conclusions of the workshop on marine mucilages in the Adriatic Sea and elsewhere. Sci Total Environ 165:9-14
49. Moran MA, Belas R, Schell MA, González JM and others (2007) Ecological genomics of marine roseobacters. Appl Environ Microbiol 73:4559-4569
50. Müller-Niklas S, Schuster S, Kaltenböck E, Herndl GJ (1994) Organic content and bacterial metabolism in amorphous aggregations of the Northern Adriatic Sea. Limnol Oceanogr 39:58-68
51. Myklestad SM (1999) Phytoplankton extracellular production and leakage with considerations on the polysaccharide accumulation. Ann Ist Super Sanit 35:401-404
52. Nagata T (2000) Production mechanisms of dissolved organic matter. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, New York, NY, p 121-152
53. Nagata T, Meon B, Kirchman DL (2003) Microbial degradation of peptidoglycan in seawater. Limnol Oceanogr 48:745-754
54. Najdek M, Degobbis D, Mioković D, Ivančić I (2002) Fatty acid and phytoplankton compositions of different types of mucilaginous aggregates in the northern Adriatic. J Plankton Res 24:429-441
55. Nishikida K, Hannah RW (1996) Selected applications of modern FT-IR techniques. CRC Press, Boca Raton, FL
56. Obernosterer I, Herndl GJ (1995) Phytoplankton extracellular release and bacterial growth: dependence on the inorganic N:P ratio. Mar. Ecol Prog Ser 116:247-257
57. Ogawa H, Amagai Y, Koike I, Kaiser K, Benner R (2001) Production of refractory dissolved organic matter by bacteria. Science 292:917-920
58. O'Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49-79
59. Pajdak-Stós A, Fialkowska E, Fyda J (2001) Phormidium autumnale (Cyanobacteria) defense against three ciliate grazer species. Aquat Microb Ecol 23:237-244
60. Peduzzi P, Weinbauer MG (1993) Effects of concentrating the virus-rich 2-200 μm size fraction of seawater on the formation of algal flocs (marine snow). Limnol Oceanogr 38:1562-1565
61. Penna N, Kovač N, Ricci F, Penna A, Capellacci S, Faganeli J (2009) The role of dissolved carbohydrates in the northern Adriatic macroaggregate formation. Acta Chim Slov 56:305-314
62. Ploug H, Grossart HP, Azam F, Jørgensen BB (1999) Photosynthesis, respiration, and carbon turnover in sinking marine snow from surface waters of Southern California Bight: implications for the carbon cycle in the ocean. Mar. Ecol Prog Ser 179:1-11
63. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943-948
64. Posedel N, Faganeli J (1991) Nature and sedimentation of suspended particulate matter during density stratification in shallow coastal waters (Gulf of Trieste, northern Adriatic). Mar. Ecol Prog Ser 77:135-145
65. Raghavan SR, Cipriano BH (2005) Gel formation: phase diagrams using tabletop rheology and calorimetry. In: Weiss RG, Terech P (eds) Molecular gels: materials with self-assembled fibrillar networks. Springer, Amsterdam, p 233-244
66. Rath J, Wu KY, Herndl GJ, DeLong EF (1998) High phylogenetic diversity in a marine-snow-associated bacterial assemblage. Aquat Microb Ecol 14:261-269
67. Sachs JP, Repeta DJ, Goercke R (1999) Nitrogen and carbon isotopic ratios of chlorophyll from marine phytoplankton. Geochim Cosmochim Acta 63:1431-1441
68. Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG (2002) Pseudomonas aeroginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184:1140-1154
69. Schaudinn C, Stoodley P, Kainović A, O'Keeffe T and others (2007) Bacterial biofilms, other structures seen as mainstream concepts. Microbe 2:231-237
70. Schiaparelli S, Castellano M, Povero P, Sartoni G, Cattaneo-Vietti R (2007) A benthic mucilage event in North-Western Mediterranean Sea and its possible relationships with the summer 2003 European heatwave: short-term effects on littoral rocky assemblages. PSZN I: Mar. Ecol 28:341-353
71. Simon M, Azam F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar. Ecol Prog Ser 51:201-213
72. Simon M, Grossart HP, Schweitzer B, Ploug H (2002) Microbial ecology of organic aggregates in aquatic ecosystems. Aquat Microb Ecol 28:175-211
73. Smucker RA, Dawson R (1986) Products and photosynthesis by marine phytoplankton: chitin in TCA 'protein' precipitates. J Exp Mar. Biol Ecol 104:143-152
74. Stachowitsch M, Fanuko N, Richter M (1990) Mucus aggregates in the Adriatic Sea: an overview of stages and occurrences. PSZN I: Mar. Ecol 11:327-350
75. Stoderegger KE, Herndl GJ (1999) Production of exopolymer particles by marine bacterioplankton under contrasting turbulence conditions. Mar. Ecol Prog Ser 189:9-16
76. Studer D, Humbel BM, Chiquet M (2008) Electron microscopy of high pressure frozen samples: bridging the gap between cellular ultrastructure and atomic resolution. Histochem Cell Biol 130:877-889
77. Supić N, Orlić M (1999) Seasonal and interannual variability of the northern Adriatic surface fluxes. J Mar. Syst 20:205-229
78. Svetličić V, Žutić V, Hozić Zimmermann A (2005) Biophysical scenario of giant gel formation in the Northern Adriatic Sea. Ann NY Acad Sci 1048:524-527
79. Thingstad TF, Hagström Å, Rassoulzadegan F (1997) Accumulation of degradable DOC in surface waters: Is it caused by a malfunctioning microbial loop? Limnol Oceanogr 42:398-404
80. Thingstad TF, Øvreås L, Egge JK, Løvdal T, Heldal M (2005) Use of non-limiting substrates to increase size: a generic strategy to simultaneously optimize uptake and minimize predation in pelagic osmotrophs? Ecol Lett 8:675-682
81. Trichet J, Défarge C, Tribble J, Tribble G, Sansone F (2001) Christmas Island lagoonal lakes, models for the deposition of carbonate-evaporite-organic laminated sediments. Sediment Geol 140:177-189
82. Verdugo P, Alldredge AL, Azam F, Kirchman DL, Passow U, Santschi PH (2004) The oceanic gel phase: a bridge in the DOM-POM continuum. Mar. Chem 92:67-85
83. Whiteley M, Bangera MG, Bumgarner RE, Parsek MR, Teitzel GM, Lory S, Greenberg EP (2001) Gene expression in Pseudomonas aeroginosa biofilms. Nature 413:860-864
84. Zaccone R, Caruso G, Cal C (2002) Heterotrophic bacteria in the northern Adriatic Sea: seasonal changes and ectoenzyme profile. Mar. Environ Res 54:1-19
85. 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