Characterization of marine bacteria and the activity of their enzyme systems involved in degradation of the algal storage glucan laminarin

FEMS Microbiology Ecology

Volumn 59, Issue 1, 2007, Pages 108-117

  Alderkamp, Anne Carlijn ^a,b   Van Rijssel, Marion ^a   Bolhuis, Henk ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Carbohydrate; Laminarin; Marine; Vibrio sp.

Indexed keywords

BACTERIAL ENZYME; CARBON; ENDO 1,3 BETA GLUCANASE; GLUCAN; GLUCOSE; GLUCOSIDE; LAMINARAN;

ABUNDANCE; ALGA; ALGAL BLOOM; BACTERIUM; DEGRADATION; DILUTION; ENZYME ACTIVITY; PHYLOGENETICS; PROKARYOTE;

ALGAL BLOOM; ARTICLE; ATLANTIC OCEAN; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIOPLANKTON; BACTERIUM ISOLATION; CHEMICAL BOND; CHEMICAL STRUCTURE; CONTROLLED STUDY; DEGRADATION KINETICS; DILUTION; ENZYME ACTIVITY; ENZYME SUBSTRATE; EPIFLUORESCENCE MICROSCOPE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROKARYOTE; PROTEIN EXPRESSION; VIBRIONACEAE;

BACTERIA; BACTEROIDETES; CELLULASES; GLUCANS; PHYLOGENY; PHYTOPLANKTON; POLYSACCHARIDES; PSEUDOALTEROMONAS; ROSEOBACTER; SUBSTRATE SPECIFICITY; VIBRIO; WATER MICROBIOLOGY;

ATLANTIC OCEAN; NORTH SEA;

ALGAE; BACTERIA (MICROORGANISMS); PROKARYOTA; VIBRIO SP.;

EID: 33845671315     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2006.00219.x     Document Type: Article

References (66)

1. Alderkamp A-C, Nejstgaard JC, Verity PG, Zirbel MJ, Sazhin AF & van Rijssel M (2006) Dynamics in carbohydrate composition of Phaeocystis pouchetii colonies during spring blooms in mesocosm. J Sea Res 55: 169-181.
2. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W & Lipman DJ (1997) Gapped BLASTand PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
3. Amon RMW & Benner R (1994) Rapid cycling of high-molecular-weight dissolved organic-matter in the ocean. Nature 369: 549-552.
4. Amon RMW & Benner R (1996) Bacterial utilization of different size classes of dissolved organic matter. Limnol Oceanogr 41: 41-51.
5. Arnosti C & Holmer M (1999) Carbohydrate dynamics and contributions to the carbon budget of an organic-rich coastal sediment. Geochim Cosmochim Acta 63: 393-403.
6. Arnosti C, Durkin S & Jeffrey WH (2005) Patterns of extracellular enzyme activities among pelagic marine microbial communities: implications for cycling of dissolved organic carbon. Aquat Microb Ecol 38: 135-145.
7. Arrieta JM & Herndl GJ (2002) Changes in bacterial beta-glucosidase diversity during a coastal phytoplankton bloom. Limnol Oceanogr 47: 594-599.
8. Azam F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280: 694-696.
9. Azúa I, Unanue M, Ayo B, Artolozaga I, Arrieta JM & Iriberri J (2003) Influence of organic matter quality in the cleavage of polymers by marine bacterial communities. J Plankt Res 25: 1451-1460.
10. Bassler BL, Gibbons PJ, Yu C & Roseman S (1991) Chitin utilization by marine bacteria chemotaxis to chitin oligosaccharides by Vibrio furnissii. J Biol Chem 266: 24268-24275.
11. Benner R, Pakulski JD, McCarty M, Hedges JI & Hatcher PG (1992) Bulk chemical characteristics of dissolved organic matter in the ocean. Science 255: 1561-1564.
12. Biddanda B & Benner R (1997) Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton. Limnol Oceanogr 42: 506-518.
13. Biersmith A & Benner R (1998) Carbohydrates in phytoplankton and freshly produced dissolved organic matter. Mar Chem 63: 131-144.
14. Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72: 248-254.
15. Brussaard CPD, Riegman R, Noordeloos AAM, Cadée GC, Witte H, Kop AJ, Nieuwland G, Van Duyl FC & Bak R-PM (1995) Effects of grazing, sedimentation and phytoplankton cell lysis on the structure of a coastal pelagic food web. Mar Ecol Prog Ser 123: 259-271.
16. Brussaard CPD, Mari X, Van Bleijswijk JDL & Veldhuis MJW (2005) A mesocosm study of Phaeocystis globosa (Prymnesiophyceae) population dynamics-II. Significance for the microbial community. Harmful Algae 4: 875-893.
17. Button DK, Schut F, Quang P, Martin R & Robertson BR (1993) Viability and isolation of marine bacteria by dilution culture: theory, procedures and initial results. Appl Environ Microbiol 59: 881-891.
18. Chin WC, Orellana MV & Verdugo P (1998) Spontaneous assembly of marine dissolved organic matter into polymer gels. Nature 391: 568-572.
19. Chiovitti A, Molino P, Crawford SA, Teng RW, Spurck T & Wetherbee R (2004) The glucans extracted with warm water from diatoms are mainly derived from intracellular chrysolaminaran and not extracellular polysaccharides. Eur J Phycol 39: 117-128.
20. Cho BC & Azam F (1988) Major role of bacteria in biochemical fluxes in the ocean's interior. Nature 332: 441-443.
21. Chróst RJ (1991) Environmental control of the synthesis and activity of aquatic microbial ectoenzymes. Microbial Enzymes in Aquatic Environments (Chróst RJ, ed), pp. 29-59. Springer Verlag, New York.
22. Clarke TR & Owens NJP (1983) A simple and versatile microcomputer program for the determination of 'most probable number'. J Microbiol Meth 1: 133-137.
23. Cowie GL & Hedges JI (1984) Carbohydrate sources in a coastal marine environment. Geochim Cosmochim Acta 48: 2075-2087.
24. Driskill LE, Bauer MW & Kelly RM (1999) Synergistic interactions among beta-laminarinase, beta-1,4-glucanase, and beta-glucosidase from the hyperthermophilic archaeon Pyrococcus furiosus during hydrolysis of beta-1,4-, beta-1,3-, and mixed-linked polysaccharides. Biotechnol Bioeng 66: 51-60.
25. Eilers H, Pernthaler J & Amann R (2000a) Succession of pelagic marine bacteria during enrichment: a close look at cultivation induced shifts. Appl Environ Microbiol 66: 4634-4640.
26. Eilers H, Pernthaler J, Glöckner FO & Amann R (2000b) Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl Environ Microbiol 66: 3044-3051.
27. Ferguson RL, Buckley EN & Palumbo AV (1984) Response of marine bacterioplankton to differential filtration and confinement. Appl Environ Microbiol 47: 49-55.
28. Granum E, Kirkvold S & Myklestad SM (2002) Cellular and extracellular production of carbohydrates and amino acids by the marine diatom Skeletonema costatum: diel variations and effects of N depletion. Mar Ecol Prog Ser 242: 83-94.
29. Healey FP (1980) Slope of the Monod equation as an indicator of advantage in nutrient competition. Microb Ecol 5: 281-286.
30. Heidelberg JF, Heidelberg KB & Colwell RR (2002) Bacteria of the gamma-subclass Proteobacteria associated with zooplankton in Chesapeake Bay. Appl Environ Microbiol 68: 5498-5507.
31. Henrissat B (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280: 309-316.
32. Huq A, Colwell RR, Rahman R, Ali A, Chowdhury MAR, Parveen S, Sack DA & Russekcohen E (1990) Detection of Vibrio cholerae O1 in the aquatic environment by fluorescentmonoclonal antibody and culture methods. Appl Environ Microbiol 56: 2370-2373.
33. Janse I, van Rijssel M, Van Hall PJ, Gerwig GJ, Gottschal JC & Prins RA (1996) The storage glucan of Phaeocystis globosa (Prymnesiophyceae) cells. J Phycol 32: 382-387.
34. Janse I, van Rijssel M, Ottema A & Gottschal JC (1999) Microbial breakdown of Phaeocystis mucopolysaccharides. Limnol Oceanogr 44: 1447-1457.
35. Janse I, Zwart G, Maarel MJEC & Gottschal JC (2000) Composition of the bacterial community degrading Phaeocystis mucopolysaccharides in enrichment cultures. Aquat Microb Ecol 22: 119-133.
36. Keith SC & Arnosti C (2001) Extracellular enzyme activity in a river-bay-shelf transect: variations in polysaccharide hydrolysis rates with substrate and size class. Aquat Microb Ecol 24: 243-253.
37. Kim YR, Lee SE, Kim CM et al. (2003) Characterization and pathogenic significance of Vibrio vulnificus antigens preferentially expressed in septicemic patients. Infect Immun 71: 5461-5471.
38. Kumar S, Tamura K & Nei M(2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5: 150-163.
39. Li XB & Roseman S (2004) The chitinolytic cascade in Vibrios is regulated by chitin oligosaccharides and a two-component chitin catabolic sensor/kinase. Proc Natl Acad Sci USA 101: 627-631.
40. Liu D, Wong PTS & Dutka BJ (1973) Determination of carbohydrate in lake sediment by a modified phenol-sulfuric acid method. Water Res 7: 741-746.
41. Martinez J, Smith DC, Steward GF &Azam F (1996) Variability in ectohydrolytic enzyme activities of pelagic marine bacteria and its significance for substrate processing in the sea. Aquat Microb Ecol 10: 223-230.
42. McDougald D, Gong L, Srinivasan S, Hild E, Thompson L, Takayama K, Rice SA & Kjelleberg S (2002) Defences against oxidative stress during starvation in bacteria. Antonie Van Leeuwenhoek 81: 3-13.
43. Meeuse BJD (1962) Storage products. Physiology and Biochemistry of Algae (Lewin RA, ed), pp. 289-291. Academic Press, New York.
44. Meibom KL, Li XBB, Nielsen AT, Wu CY, Roseman S & Schoolnik GK (2004) The Vibrio cholerae chitin utilization program. Proc Nat Acad Sci USA 101: 2524-2529.
45. Middelboe M, Sondergaard M, Letarte Y & Borch NH (1995) Attached and free-living bacteria-production and polymer hydrolysis during a diatom bloom. Microb Ecol 29: 231-248.
46. Myklestad SM (1974) Production of carbohydrates by marine planktonic diatoms. I. Comparison of nine different spcies in culture. J Exp Mar Biol Ecol 15: 261-274.
47. Myklestad SM, Skanoy E & Hestmann S (1997) A sensitive and rapid method for analysis of dissolved mono- and polysaccharides in seawater. Mar Chem 56: 279-286.
48. Møller EF, Thor P & Nielsen TG (2003) Production of DOC by Calanus finmarchicus, C. glacialis and C. hyperboreus through sloppy feeding and leakage from fecal pellets. Mar Ecol Prog Ser 262: 185-191.
49. Nelson DM, Treguer P, Brzezinski MA, Leynaert A & Queguiner B (1995) Production and dissolution of biogenic silica in the ocean-revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochem Cycles 9: 359-372.
50. Noordkamp DJB, Gieskes WWC, Gottschal JC, Forney LJ & van Rijssel M (2000) Acrylate in Phaeocystis colonies does not affect the surrounding bacteria. J Sea Res 43: 287-296.
51. Nyström T, Olsson RM & Kjelleberg S (1992) Survival, stress resistance, and alterations in protein expression in the marine Vibrio sp. stain S14 during starvation for different individual nutrients. Appl Environ Microbiol 58: 55-65.
52. Oliver JD, Nilsson L & Kjelleberg S (1991) Formation of nonculturable Vibrio vulnificus cells and its relationship to the starvation state. Appl Environ Microbiol 57: 2640-2644.
53. Painter TJ (1983) Algal polysaccharides. The Polysaccharides (Aspinall GO, ed), pp. 195-285. Academic Press, New York.
54. Paul JH (1982) Use of Hoechst Dyes 33258 and 33342 for enumeration of attached and planktonic bacteria. Appl Environ Microbiol 43: 939-944.
55. Pinhassi J, Sala MM, Havskum H, Peters F, Guadayol O, Malits A & Marrase CL (2004) Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microbiol 70: 6753-6766.
56. Read SM, Currie G & Bacic A (1996) Analysis of the structural heterogeneity of laminarin by electrospray-ionisation-mass spectrometry. Carbohydr Res 281: 187-201.
57. Sambrook J, Fritsch EF & Maniatis T (1989) Molecular Cloning: a Laboratory Manual. Cold Spring Harbour Laboratory Press, Cold Spring Harbour, NY.
58. Schoemann W, Becquevort S, Stefels J, Rousseau W & Lancelot C (2005) Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J Sea Res 53: 43-66.
59. Smith DC, Simon M, Alldredge AL & Azam F (1992) Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 359: 139-141.
60. Smith DC, Steward GF, Long RA & Azam F (1995) Bacterial mediation of carbon fluxes during a diatom bloom in a mesocosm. Deep Sea Res II 42: 75-97.
61. Uchida M (1995) Enzyme activities of marine bacteria involved in Laminaria-thallus decomposition and the resulting sugar release. Mar Biol 123: 639-644.
62. Unanue M, Azúa I, Arrieta JM, Labirua IA, Egea L & Iriberri J (1998) Bacterial colonization and ectoenzymatic activity in phytoplankton- derived model particles: cleavage of peptides and uptake of amino acids. Microb Ecol 35: 136-146.
63. Utermohl H (1958) Zur Vervollkomnung der quantitativen Phytoplankton-Methodik. Mitt Int Ver Limnol 9: 1-38.
64. 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.
65. Warren RAJ (1996) Microbial hydrolysis of polysaccharides. Annu Rev Microbiol 50: 183-212.
66. Weiss MS, Abele U, Weckesser J, Welte W, Schiltz E & Schulz GE (1991) Molecular architecture and electrostatic properties of a bacterial porin. Science 254: 1627-1630.