High Contribution of SAR11 to Microbial Activity in the North West Mediterranean Sea

Microbial Ecology

Volumn 63, Issue 2, 2012, Pages 324-333

  Laghdass, Mélissa ^a,b   Catala, Philippe ^a,b   Caparros, Jocelyne ^a,b   Oriol, Louise ^a,b   Lebaron, Philippe ^a,b   Obernosterer, Ingrid ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b LABORATOIRE ARAGO   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; ADENOSINE TRIPHOSPHATE; AMINO ACID; CARBON; GLUCOSE; INDOLE DERIVATIVE; LEUCINE; NITROGEN; PHOSPHORUS; SEA WATER;

ALPHAPROTEOBACTERIA; ARTICLE; AUTORADIOGRAPHY; CHEMISTRY; ECOSYSTEM; FLUORESCENCE IN SITU HYBRIDIZATION; FRANCE; GROWTH, DEVELOPMENT AND AGING; MEDITERRANEAN SEA; METABOLISM; MICROBIOLOGY; SEASON;

ADENOSINE TRIPHOSPHATE; ALPHAPROTEOBACTERIA; AMINO ACIDS; AUTORADIOGRAPHY; CARBON; ECOSYSTEM; FRANCE; GLUCOSE; IN SITU HYBRIDIZATION, FLUORESCENCE; INDOLES; LEUCINE; MEDITERRANEAN SEA; NITROGEN; PHOSPHORUS; SEASONS; SEAWATER;

BACTERIA (MICROORGANISMS);

EID: 84856692193     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-011-9915-7     Document Type: Article

References (63)

1. Carlson C (2002) Production and removal processes. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic, San Diego.
2. Thingstad T, Zweifel U, Rassoulzadegan F (1998) P limitation of heterotrophic bacteria and phytoplankton in the northwest Mediterranean. Limnol Oceanogr 43: 88-94.
3. Joint I, Henriksen P, Fonnes GA, Bourne D, Thingstad TF, Riemann B (2002) Competition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms. Aquat Microb Ecol 29: 145-159.
4. Teira E, Martínez-García S, Carreira C, Morán XAG (2011) Changes in bacterioplankton and phytoplankton community composition in response to nutrient additions in coastal waters off the NW Iberian Peninsula. Mar Ecol Prog Ser 426: 87-104.
5. Pinhassi J, Gómez-Consarnau L, Alonso-Sáez L, Sala M, Vidal M, Pedrós-Alió C, Gasol J (2006) Seasonal changes in bacterioplankton nutrient limitation and their effects on bacterial community composition in the NW Mediterranean Sea. Aquat Microb Ecol 44: 241-252.
6. Zohary T, Robarts R (1998) Experimental study of microbial P limitation in the eastern Mediterranean. Limnol Oceanogr 43: 387-395.
7. van Wambeke F, Christaki 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.
8. Cotner J, Ammerman J, Peele E, Bentzen E (1997) Phosphorus-limited bacterioplankton growth in the Sargasso Sea. Aquat Microb Ecol 13: 141-149.
9. Obernosterer I, Kawasaki N, Benner R (2003) P-limitation of respiration in the Sargasso Sea and uncoupling of bacteria from P-regeneration in size-fractionation experiments. Aquat Microb Ecol 32: 229-237.
10. van Wambeke F, Obernosterer I, Moutin T, Duhamel S, Ulloa O, Claustre H (2008) Heterotrophic bacterial production in the eastern South Pacific: longitudinal trends and coupling with primary production. Biogeosciences 5: 157-169.
11. Rivkin R, Anderson M (1997) Inorganic nutrient limitation of oceanic bacterioplankton. Limnol Oceanogr 42: 730-740.
12. Carlson CA, Ducklow HW (1996) Growth of bacterioplankton and consumption of dissolved organic carbon in the Sargasso Sea. Aquat Microb Ecol 10: 69-85.
13. Kirchman D, Rich J (1997) Regulation of bacterial growth rates by dissolved organic carbon and temperature in the equatorial Pacific Ocean. Microb Ecol 33: 11-20.
14. Elifantz H, Malmstrom R, Cottrell M, Kirchman D (2005) Assimilation of polysaccharides and glucose by major bacterial groups in the Delaware Estuary. Appl Environ Microb 71: 7799-7805.
15. Teira E, Lebaron P, van Aken H, Herndl G (2006) Distribution and activity of Bacteria and Archaea in the deep water masses of the North Atlantic. Limnol Oceanogr 51: 2131.
16. Cottrell M, Kirchman D (2000) Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol 66: 1692-1697.
17. Alonso-Sáez L, Gasol JM (2007) Seasonal variations in the contributions of different bacterial groups to the uptake of low-molecular-weight compounds in northwestern Mediterranean coastal waters. Appl Environ Microbiol 73: 3528-3535.
18. Zubkov M, Mary I, Woodward E, Warwick P, Fuchs B, Scanlan D, Burkill P (2007) Microbial control of phosphate in the nutrient-depleted North Atlantic subtropical gyre. Environ Microbiol 9: 2079-2089.
19. Longnecker K, Lomas M, van Mooy B (2010) Abundance and diversity of heterotrophic bacterial cells assimilating phosphate in the subtropical North Atlantic Ocean. Environ Microbiol 2: 2773-2782.
20. Morris RM, Rappé MS, Connon SA, Vergin KL, Siebold WA, Carlson CA, Giovannoni SJ (2002) SAR 11 clade dominates ocean surface bacterioplankton communities. Nature 420: 806-810.
21. Mary I, Heywood J, Fuchs B, Amann R, Tarran G, Burkill P, Zubkov M (2006) SAR11 dominance among metabolically active low nucleic acid bacterioplankton in surface waters along an Atlantic meridional transect. Aquat Microb Ecol 45: 107-113.
22. Malmstrom RR, Kiene RP, Cottrell MT, Kirchman DL (2004) Contribution of SAR11 bacteria to dissolved dimethylsulfoniopropionate and amino acid uptake in the North Atlantic ocean. Appl Environ Microbiol 70: 4129-4135.
23. Vila-Costa M, Pinhassi J, Alonso C, Pernthaler J, Simo R (2007) An annual cycle of dimethylsulfoniopropionate-sulfur and leucine assimilating bacterioplankton in the coastal NW Mediterranean. Environ Microbiol 9: 2451-2463.
24. Wilhelm L, Tripp H, Givan S, Smith D, Giovannoni S (2007) Natural variation in SAR 11 marine bacterioplankton genomes inferred from metagenomic data. Biology Direct 2: 27.
25. Sowell S, Wilhelm L, Norbeck A, Lipton M, Nicora C, Barofsky D, Carlson C, Smith R, Giovannoni S (2008) Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea. The ISME Journal 3: 93-105.
26. Giovannoni S, Bibbs L, Cho J, Stapels M, Desiderio R, Vergin K, Rappé M, Laney S, Wilhelm L, Tripp H (2005) Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438: 82-85.
27. Gilbert J, Mühling M, Joint I (2008) A rare SAR11 fosmid clone confirming genetic variability in the 'Candidatus Pelagibacter ubique'genome. The ISME Journal 2: 790-793.
28. Lami R, Cottrell M, Campbell B, Kirchman D (2009) Light-dependent growth and proteorhodopsin expression by Flavobacteria and SAR11 in experiments with Delaware coastal waters. Environ Microbiol 11: 3201-3209.
29. Laghdass M, West NJ, Batailler N, Caparros J, Catala P, Lantoine F, Oriol L, Lebaron P, Obernosterer I (2010) Impact of lower salinity waters on bacterial heterotrophic production and community structure in the offshore NW Mediterranean Sea. Environ Microbiol Rep 2: 761-769.
30. Tréguer P, Le Corre P (1975) Manuel d'analyse des sels nutritifs dans l'eau de mer. Laboratoire d'Océanographie Chimique, Université de Bretagne Occidentale, Brest, p 110.
31. Pujo-Pay M, Raimbault P (1994) Improvement of the wet-oxidation procedure for simultaneous determination of particulate organic nitrogen and phosphorus collected on filters. Mar Ecol Prog Ser 105: 203-207.
32. Benner R, Strom M (1993) A critical evaluation of the analytical blank associated with DOC measurements by high-temperature catalytic oxidation. Mar Chem 41: 153-160.
33. Pernthaler A, Pernthaler J, Amann R (2002) Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol 68: 3094-3101.
34. Sekar R, Pernthaler A, Pernthaler J, Warnecke F, Posch T, Amann R (2003) An improved protocol for quantification of freshwater Actinobacteria by fluorescence in situ hybridization. Appl Environ Microbiol 69: 2928-2935.
35. Amann R, Krumholz L, Stahl D (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172: 762-770.
36. Daims H, Brühl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB 338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22: 434-444.
37. Glöckner FO, Fuchs BM, Amann R (1999) Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65: 3721-3726.
38. Cottrell MT, Kirchman DL (2003) Contribution of major bacterial groups to bacterial biomass production (thymidine and leucine incorporation) in the Delaware estuary. Limnol Oceanogr 48: 168-178.
39. Lebaron P, Parthuisot N, Catala P (1998) Comparison of blue nucleic acid dyes for flow cytometric enumeration of bacteria in aquatic systems. Appl Environ Microbiol 64: 1725-1730.
40. 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 Microb 64: 3352-3358.
41. 3H-leucine. Mar Microb Food Webs 6: 107-114.
42. Kirchman D (1993) Leucine incorporation as a measure of biomass production by heterotrophic bacteria. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods in aquatic microbial ecology. Lewis, Boca Raton, pp 509-512.
43. Lemée R, Rochelle-Newall E, van Wambeke F, Pizay MD, Rinaldi P, Gattuso JP (2002) Seasonal variation of bacterial production, respiration and growth efficiency in the open NW Mediterranean Sea. Aquat Microb Ecol 29: 227-237.
44. Lami R, Ghiglione JF, Desdevises Y, West NJ, Lebaron P (2009) Annual patterns of presence and activity of marine bacteria monitored by 16S rDNA-16S rRNA fingerprints in the coastal NW Mediterranean Sea. Aquat Microb Ecol 54: 199-210.
45. Tanaka T, Rassoulzadegan F, Thingstad T (2004) Orthophosphate uptake by heterotrophic bacteria, cyanobacteria, and autotrophic nanoflagellates in Villefranche Bay, northwestern Mediterranean: vertical, seasonal, and short-term variations of the competitive relationship for phosphorus. Limnol Oceanogr 49: 1063-1072.
46. Thingstad T, Krom M, Mantoura R, Flaten G, Groom S, Herut B, Kress N, Law C, Pasternak A, Pitta P (2006) Nature of phosphorus limitation in the ultraoligotrophic eastern Mediterranean. Science 309: 1068.
47. Dolan J, Thingstad T, Rassoulzadegan F (1995) Phosphate transfer between microbial size-fractions in Villefranche Bay (NW Mediterranean Sea), France in autumn 1992. Ophelia 41: 71-85.
48. Copin-Montégut G, Avril B (1993) Vertical distribution and temporal variation of dissolved organic carbon in the North-Western Mediterranean Sea. Deep-Sea Res I 40: 1963-1972.
49. Carlson C, Giovannoni S, Hansell D, Goldberg S, Parsons R, Otero M, Vergin K, Wheeler B (2002) Effect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea. Aquat Microb Ecol 30: 19-36.
50. Alonso-Sáez L, Balagué V, Sa EL, Sanchez O, Gonzalez JM, Pinhassi J, Massana R, Pernthaler J, Pedrós-Alió C, Gasol JM (2007) Seasonality in bacterial diversity in north-west Mediterranean coastal waters: assessment through clone libraries, fingerprinting and FISH. FEMS Microbiol Ecol 60: 98-112.
51. Malmstrom RR, Cottrell MT, Elifantz H, Kirchman DL (2005) Biomass production and assimilation of dissolved organic matter by SAR11 bacteria in the Northwest Atlantic Ocean. Appl Environ Microbiol 71: 2979-2986.
52. Teira E, Martínez-García S, Lønborg C, Álvarez-Salgado X (2009) Growth rates of different phylogenetic bacterioplankton groups in a coastal upwelling system. Environ Microbiol Rep 1: 545-554.
53. Rappé M, Connon S, Vergin K, Giovannoni S (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418: 630-633.
54. Hamasaki K, Taniguchi A, Tada Y, Long RA, Azam F (2007) Actively growing bacteria in the Inland Sea of Japan, identified by combined bromodeoxyuridine immunocapture and denaturing gradient gel electrophoresis. Appl Environ microb 73: 2787.
55. Alonso C, Pernthaler J (2006) Roseobacter and SAR11 dominate microbial glucose uptake in coastal North Sea waters. Environ Microbiol 8: 2022-2030.
56. Malmstrom R, Kiene R, Kirchman D (2004) Identification and enumeration of bacteria assimilating dimethylsulfoniopropionate (DMSP) in the North Atlantic and Gulf of Mexico. Limnol Oceanogr 49: 597-606.
57. Carlson CA, Morris R, Parsons R, Treusch AH, Giovannoni SJ, Vergin K (2009) Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea. The ISME Journal 3: 283-295.
58. Alonso-Sáez L, Sanchez O, Gasol J, Balagué V, Pedrós-Alió C (2008) Winter-to-summer changes in the composition and single-cell activity of near-surface Arctic prokaryotes. Environ Microbiol 10: 2444-2454.
59. Sintes E, Herndl GJ (2006) Quantifying substrate uptake by individual cells of marine bacterioplankton by catalyzed reporter deposition fluorescence in situ hybridization combined with microautoradiography? Appl Environ Microbiol 72: 7022-7028.
60. Garcia-Martinez J, Rodriguez-Valera F (2000) Microdiversity of uncultured marine prokaryotes: the SAR11 cluster and the marine Archaea of Group I. Mol Ecol 9: 935-948.
61. Schwalbach M, Tripp H, Steindler L, Smith D, Giovannoni S (2010) The presence of the glycolysis operon in SAR11 genomes is positively correlated with ocean productivity. Environ Microbiol 12: 490-500.
62. Lauro FM, McDougald D, Thomas T, Williams TJ, Egan S, Rice S, DeMaere MZ, Ting L, Ertan H, Johnson J, Ferriera S, Lapidus A, Anderson I, Kyrpides N, Munk AC, Detter C, Han CS, Brown MV, Robb FT, Kjelleberg S, Cavicchioli R (2009) The genomic basis of trophic strategy in marine bacteria. PNAS 106: 15527-15533.
63. Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL, Baptista D, Bibbs L, Eads J, Richardson TH, Noordewier M, Rappe MS, Short JM, Carrington JC, Mathur EJ (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science 309: 1242-1245.