Spatial and temporal variability among marine Bacteroidetes populations in the NW Mediterranean Sea

Systematic and Applied Microbiology

Volumn 37, Issue 1, 2014, Pages 68-78

  Díez Vives, Cristina ^a   Gasol, Josep M ^a   Acinas, Silvia G ^a  

^a INSTITUT DE CIÈNCIES DEL MAR   (Spain)

Author keywords

Bacteroidetes populations; CARD FISH; DGGE; Diversity; Spatial and temporal variability; Structure

Indexed keywords

BACTEROIDETES POPULATIONS; CARD-FISH; DGGE; DIVERSITY; SPATIAL AND TEMPORAL VARIABILITY; STRUCTURE;

BACTEROIDETES; BIODIVERSITY; CLUSTER ANALYSIS; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA, BACTERIAL; DNA, RIBOSOMAL; GENETIC VARIATION; GEOGRAPHY; MEDITERRANEAN SEA; MOLECULAR SEQUENCE DATA; RNA, RIBOSOMAL, 16S; SEASONS; SEAWATER; SEQUENCE ANALYSIS, DNA; TIME FACTORS;

EID: 84895067499     PISSN: 07232020     EISSN: 16180984     Source Type: Journal    
DOI: 10.1016/j.syapm.2013.08.006     Document Type: Article

References (80)

1. Abell G.C.J., Bowman J.P. Colonization and community dynamics of class Flavobacteria on diatom detritus in experimental mesocosms based on Southern Ocean seawater. FEMS Microbiol. Ecol. 2005, 53:379-391.
2. Acinas S.G., Rodríguez-Valera F., Pedrós-Alió C. Spatial and temporal variation in marine bacterioplankton diversity as shown by RFLP fingerprinting of PCR amplified 16S rDNA. FEMS Microbiol. Ecol. 1997, 24:27-40.
3. Alderkamp A.C., Sintes E., Herndl G.J. Abundance and activity of major groups of prokaryotic plankton in the coastal North Sea during spring and summer. Aquatic Microbial Ecology 2006, 45:237-246.
4. Alonso C., Warnecke F., Amann R., Pernthaler J. High local and global diversity of Flavobacteria in marine plankton. Environ. Microbiol. 2007, 9:1253-1266.
5. Alonso-Sáez L., Gasol J.M., Lefort T., Hofer J., Sommaruga R. Effect of natural sunlight on bacterial activity and differential sensitivity of natural bacterioplankton groups in northwestern Mediterranean coastal waters. Appl. Environ. Microbiol. 2006, 72:5806-5813.
6. Alonso-Sáez L., Vázquez-Domínguez E., Cardelús C., Pinhassi J., Sala M., Lekunberri I., Balagué V., Vila-Costa M., Unrein F., Massana R., Simó R., Gasol J.M. Factors controlling the year-round variability in carbon flux through bacteria in a coastal marine system. Ecosystems 2008, 11:397-409.
7. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool (BLAST). J. Mol. Biol. 1990, 215:403-410.
8. Amann R.I., Fuchs B.M. Single cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nat. Rev. Microbiol. 2008, 6:339-348.
9. Bano N., Hollibaugh J.T. Phylogenetic composition of bacterioplankton assemblages from the Arctic Ocean. Appl. Environ. Microbiol. 2002, 68:505-518.
10. Bauer M., Kube M., Teeling H., Richter M., Lombardot T., Allers E., Würdemann C.A., Quast C., Kuhl H., Knaust F., Woebken D., Bischof K., Mussmann M., Choudhuri J.V., Meyer F., Reinhardt R., Amann R., Glöckner F.O. Whole genome analysis of the marine Bacteroidetes 'Gramella forsetii' reveals adaptations to degradation of polymeric organic matter. Environ. Microbiol. 2006, 8:2201-2213.
11. Béjà O., Koonin E.V., Aravind L., Taylor L.T., Seitz H., Stein J.L., Bensen D.C., Feldman R.A., Swanson R.V., Delong E.F. Comparative genomic analysis of archaeal genotypic variants in a single population and in two different oceanic provinces. Appl. Environ. Microbiol. 2002, 68:335-345.
12. Blümel M., Süling J., Imhoff J.F. Depth-specific distribution of Bacteroidetes in the oligotrophic eastern Mediterranean Sea. Aquat. Microb. Ecol. 2007, 46:209-224.
13. Brinkmeyer R., Knittel K., Jürgens J., Weyland H., Amann R., Helmke E. Diversity and structure of bacterial communities in Arctic versus Antarctic pack ice. Appl. Environ. Microbiol. 2003, 69:6610-6619.
14. Casamayor E.O., Pedrós-Alió C., Muyzer G., Amann R. Microheterogeneity in 16S ribosomal DNA-defined bacterial populations from a stratified planktonic environment is related to temporal changes and to ecological adaptations. Appl. Environ. Microbiol. 2002, 68:1706-1714.
15. Chen X., Zeng Y., Jiao N. Development and evaluation of specific 16S rDNA primers for marine Cytophaga-Flavobacteria cluster. Mol. Ecol. Notes 2006, 6:1278-1281.
16. Cottrell M., Kirchman D. Community composition of marine bacterioplankton determined by 16S rRNA gene clone libraries and fluorescence in situ hybridization. Appl. Environ. Microbiol. 2000, 66:5116-5122.
17. Cottrell M., Kirchman D. Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular weight dissolved organic matter. Appl. Environ. Microbiol. 2000, 66:1692-1697.
18. Crespo B.G., Pommier T., Fernández-Gómez B., Pedrós-Alió C. Taxonomic composition of the particle attached and free-living bacterial assemblages in the Northwest Mediterranean Sea analyzed by pyrosequencing of the 16S rRNA. Microbiology Open 2013, 2:541-552.
19. Crump B.C., Armbrust E.V., Baross J.A. Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal ocean. Appl. Environ. Microbiol. 1999, 65:3192-3204.
20. De Gregoris T.B., Aldred N., Clare A.S., Burgess J.G. Improvement of phylum- and class-specific primers for real-time PCR quantification of bacterial taxa. J. Microbiol. Methods 2011, 86:351-356.
21. Delong E.F., Franks D.G., Alldredge A.L. Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol. Oceanogr. 1993, 38:924-934.
22. Díez-Vives C., Gasol J.M., Acinas S.G. Evaluation of marine Bacteroidetes-specific primers for microbial diversity and dynamics studies. Microb. Ecol. 2012, 64:1047-1055.
23. Doval M.D., Álvarez-Salgado X.A., Gasol J.M., Lorenzo L.M., Mirón I., Figueiras F.G., Pedrós-Alió C. Dissolved and suspended organic carbon in the Atlantic sector of the Southern Ocean, Stock dynamics in upper ocean waters. Mar. Ecol. Prog. Ser. 2001, 223:27-38.
24. Eilers H., Pernthaler J., Glockner F., Amann R. Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl. Environ. Microbiol. 2000, 66:3044-3051.
25. Eilers H., Pernthaler J., Peplies J., Glöckner F.O., Gerdts G., Amann R. Isolation of novel pelagic bacteria from the German Bight and their seasonal contributions to surface picoplankton. Appl. Environ. Microbiol. 2001, 67:5134-5142.
26. Estrada M., Salat J. Phytoplankton assemblages of deep and surface water layers in a Mediterranean frontal zone. Sci. Mar. 1989, 53:203-214.
27. Estrada M., Marrasé C., Latasa M., Berdalet E. Variability of deep chlorophyll maximum characteristics in the Northwestern Mediterranean. Mar. Ecol. Prog. Ser. 1993, 92:289-300.
28. Estrada M., Varela R.A., Salat J., Cruzado A., Arias E. Spatio-temporal variability of the winter phytoplankton distribution across the Catalan and North Balearic fronts (NW Mediterranean). J. Plankton Res. 1999, 21:1-20.
29. Fandino L.B., Riemann L., Steward G.F., Long R.A., Azam F. Variations in bacterial community structure during a dinoflagellate bloom analyzed by DGGE and 16S rDNA sequencing. Aquat. Microb. Ecol. 2001, 23:119-130.
30. Fandino L.B., Riemann L., Steward G.F., Azam F. Population dynamics of Cytophaga-Flavobacteria during marine phytoplankton blooms analyzed by real-time quantitative PCR. Aquat. Microb. Ecol. 2005, 40:251-257.
31. Fernández-Gómez B., Richter M., Schüler M., Pinhassi J., Acinas S.G., González J.M., Pedrós-Alió C. Ecology of marine Bacteroidetes: a comparative genomics approach. ISME J. 2013, 7:1-12.
32. Gasol J.M., Del Giorgio P.A. Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci. Mar. 2000, 64:197-224.
33. Gasol J.M., Doval M.D., Pinhassi J., Calderón-Paz J.I., Guixa-Boixareu N., Vaqué D., Pedrós-Alió C. Diel variations in bacterial heterotrophic activity and growth in the northwestern Mediterranean Sea. Mar. Ecol. Prog. Ser. 1998, 164:107-124.
34. Gasol J.M., Massana R., Simó R., Marrasé C., Acinas S.G., Pedrós-Alió C., Pelejero C., Sala M.M., Calvo E., Vaqué D., Peters F. Blanes Bay (site 55). ICES Phytoplankton and Microbial Plankton Status Report 2009/2010. ICES Cooperative Research Report No. 313 2012, 138-141. 196 pp. T.D. O'Brien, W.K.W. Li, X.A.G. Morán (Eds.).
35. Ghiglione J.F., Larcher M., Lebaron P. Spatial and temporal scales of variation in bacterioplankton community structure in the NW Mediterranean Sea. Aquat. Microb. Ecol. 2005, 40:229-240.
36. Gilbert J.A., Steele J.A., Caporaso J.G., Steinbrück L., Reeder J., Temperton B., Huse S., McHardy A.C., Knight R., Joint I., Somerfield P., Fuhrman J.A., Field D. Defining seasonal marine microbial community dynamics. ISME J. 2012, 6:298-308.
37. Glöckner F.O., Fuchs B.M., Amann R. Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl. Environ. Microbiol. 1999, 64:3721-3726.
38. Gómez-Pereira P.R., Fuchs B.M., Alonso C., Oliver M.J., van Beusekom J.E., Amann R. Distinct flavobacterial communities in contrasting water masses of the North Atlantic Ocean. ISME J. 2010, 4:472-487.
39. González J.M., Fernández-Gómez B., Fernàndez-Guerra A., Gomez-Consarnau L., Sánchez O., Coll-Lladó M., del Campo J., Escudero L., Rodríguez-Martínez R., Alonso-Sáez L., Latasa M., Paulsen I., Nedashkovskaya O., Lekunberri I., Pinhassi J., Pedrós-Alió C. Genome analysis of the proteorhodopsin-containing marine bacterium Polaribacter sp. MED152 (Flavobacteria). Proc. Natl. Acad. Sci. USA 2008, 105:8724-8729.
40. Guixa-Boixereu N., Vaqué D., Gasol J.M., Pedrós-Alió C. Distribution of viruses and their potential effect on bacterioplankton in an oligotrophic marine system. Aquat. Microb. Ecol. 1999, 19:205-213.
41. Jaspers E., Overmann J. Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl. Environ. Microbiol. 2004, 70:4831-4839.
42. Jaspers E., Nauhaus K., Cypionka H., Overmann J. Multitude and temporal variability of ecological niches as indicated by the diversity of cultivated bacterioplankton. FEMS Microbiol. Ecol. 2001, 36:153-164.
43. Kan J., Wang K., Chen F. Temporal variation and detection limit of an estuarine bacterioplankton community analyzed by denaturing gradient gel electrophoresis (DGGE). Aquat. Microb. Ecol. 2006, 42:7-18.
44. Kirchman D.L. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol. Ecol. 2002, 39:91-100.
45. Kirchman D.L., Yu L., Cottrell M.T. Diversity and abundance of uncultured Cytophaga-like bacteria in the Delaware Estuary. Appl. Environ. Microbiol. 2003, 69:6587-6596.
46. Kirchman D.L., Dittel A.I., Malmstrom R.R., Cottrell M.T. Biogeography of major bacterial groups in the Delaware Estuary. Limnol. Oceanogr. 2005, 50:1697-1706.
47. Lau K.W.K., Ng C.Y.M., Ren J., Lau S.C.L., Qian P.Y., Wong P.K., Lau T.C., Wu M. Owenweeksia hongkongensis gen. nov., sp. nov., a novel marine bacterium of the phylum 'Bacteroidetes'. Int. J. Syst. Evol. Microbiol. 2005, 55:1051-1057.
48. Lee S., Fuhrman J.A. Spatial and temporal variation of natural bacterioplankton assemblages studied by total genomic DNA cross-hybridization. Limnol. Oceanogr. 1991, 36:1277-1287.
49. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Yadhukumar A., Buchner T., Lai S., Steppi G., Jobb W., Förster I., Brettske S., Gerber A.W., Ginhart O., Gross S., Grumann S., Hermann R., Jost A., König T., Liss R., Lüßmann M., May B., Nonhoff B., Reichel R., Strehlow A., Stamatakis N., Stuckmann A., Vilbig M., Lenke T., Ludwig A., Bode K.H., Schleifer ARB: a software environment for sequence data. Nucleic Acids Res. 2004, 32:1363-1371.
50. Ludwig W., Euzéby J., Whitman W.B. Road map of the phyla Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes. Bergey's Manual of Systematic Bacteriology 2010, vol. 4:1-19. Springer-Verlag, New York, NY, USA. 2nd ed.
51. Malmstrom R.R., Straza T.R.A., Cottrell M.T., Kirchman D.L. Diversity, abundance, and biomass production of bacterial groups in the western Arctic Ocean. Aquat. Microb. Ecol. 2007, 47:45-55.
52. Marie D., Partensky F., Jacquet S., Vaulot D. Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl. Environ. Microbiol. 1997, 63:186-193.
53. Mary I., Cummings D.G., Biegala I.C., Burkill P.H., Archer S.D., Zubkov M.V. Seasonal dynamics of bacterioplankton community structure at a coastal station in the western English Channel. Aquat. Microb. Ecol. 2006, 41:119-126.
54. Massana R., Murray A.E., Preston C.M., Delong E.F. Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl. Environ. Microbiol. 1997, 63:50-56.
55. Moeseneder M.M., Winter C., Herndl G.J. Horizontal and vertical complexity of attached and free-living bacteria of the eastern Mediterranean Sea, determined by 16S rDNA and 16S rRNA fingerprints. Limnol. Oceanogr. 2001, 46:95-107.
56. Muyzer G., Brinkhoff T.T., Nübel U., Santegoeds C., Schäfer H., Wawer C. Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. Molecular Microbial Ecology Manual 1998, 3.4.4/1-3.4.4/27. Kluwer, Dordrecht. A.D.L. Akkermans, J.D. van Elsas, F.J. Bruijn (Eds.).
57. O'Sullivan L.A., Fuller K.E., Thomas E.M., Turley C.M., Fry J.C., Weightman A.J. Distribution and culturability of the uncultivated 'AGG58 cluster' of the Bacteroidetes phylum in aquatic environments. FEMS Microbiol. Ecol. 2004, 47:359-370.
58. Pedrós-Alió C., Calderón-Paz J.-I., Guixa-Boixereu N., Estrada M., Gasol J.M. Bacterioplankton and phytoplankton biomass and production during summer stratification in the northwestern Mediterranean Sea. Deep Sea Res. Part I: Oceanogr. Res. Pap. 1999, 46:985-1019.
59. Pernthaler A., Pernthaler J., Amann R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 2002, 68:3094-3101.
60. Pinhassi J., Hagström A. Seasonal succession in marine bacterioplankton. Aquat. Microb. Ecol. 2000, 21:245-256.
61. Pinhassi J., Sala M.M., Havskum H., Peters F., Guadayol Ò., Malits A., Marrasé C. Changes in bacterioplankton composition under different phytoplankton regimens. Appl. Environ. Microbiol. 2004, 70:6753.
62. Pommier T., Neal P., Gasol J.M., Coll M., Acinas S.G., Pedrós-Alió C. Spatial patterns of bacterial richness and evenness in the NW Mediterranean Sea explored by pyrosequencing of the 16S rRNA. Aquat. Microb. Ecol. 2010, 61:221-233.
63. Riemann L., Middelboe M. Stability of bacterial and viral community compositions in Danish coastal waters as depicted by DNA fingerprinting techniques. Aquat. Microb. Ecol. 2002, 27:219-232.
64. Riemann L., Winding A. Community dynamics of free-living and particle-associated bacterial assemblages during a freshwater phytoplankton bloom. Microb. Ecol. 2001, 42:274-285.
65. Riemann L., Steward G., Fandino L., Campbell L., Landry M., Azam F. Bacterial community composition during two consecutive NE Monsoon periods in the Arabian Sea studied by denaturing gradient gel electrophoresis (DGGE) of rRNA genes. Deep-Sea Res. Part II: Topical Stud Oceanogr. 1999, 46:1791-1811.
66. Rink B., Seeberger S., Martens T., Duerselen C.-D., Simon M., Brinkhoff T. Effects of phytoplankton bloom in a coastal ecosystem on the composition of bacterial communities. Aquat. Microb. Ecol. 2007, 48:47-60.
67. Rink B., Martens T., Fischer D., Lemke A., Grossart H.-P., Simon M., Brinkhoff T. Short-term dynamics of bacterial communities in a tidally affected coastal ecosystem. FEMS Microbiol. Ecol. 2008, 66:306-319.
68. Ruiz-González C., Lefort T., Galí M., Montserrat Sala M., Sommaruga R., Simó R., Gasol J.M. Seasonal patterns in the sunlight sensitivity of bacterioplankton from Mediterranean surface coastal waters. FEMS Microbiol. Ecol. 2011, 79:661-674.
69. Salat J. Review of hydrographic environmental factors that may influence anchovy habitats in northwestern Mediterranean. Sci. Mar. 1996, 60:21-32.
70. Schattenhofer M., Fuchs B.M., Amann R., Zubkov M.V., Tarran G.A., Pernthaler J. Latitudinal distribution of prokaryotic picoplankton populations in the Atlantic Ocean. Environ. Microbiol. 2009, 11:2078-2093.
71. Schauer M., Balagué V., Pedrós-Alió C., Massana R. Seasonal changes in the taxonomic composition of bacterioplankton in a coastal oligotrophic system. Aquat. Microb. Ecol. 2003, 31:163-174.
72. Simon M., Glöckner O., Amann R. Different community structure and temperature optima of heterotrophic picoplankton in various regions of the Southern Ocean. Aquat. Microb. Ecol. 1999, 18:275-284.
73. Sokal R.R., Rohlf F.J. Biometry 1995, W.H. Freeman & Company, New York. 3rd ed.
74. Suzuki M., Nakagawa Y., Harayama S., Yamamoto S. Phylogenetic analysis and taxonomic study of marine Cytophaga-like bacteria: proposal for Tenacibaculum gen. nov. with Tenacibaculum maritimum comb. nov. and Tenacibaculum ovolyticum comb. nov., and description of Tenacibaculum mesophilum sp. nov. and Tenacibaculum amylolyticum sp. nov. Int. J. Syst. Evol. Microbiol. 2001, 51:1639-1652.
75. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
76. Teeling H., Fuchs B.M., Becher D., Klockow C., Gardebrecht A., Bennke C.M., Kassabgy M., Huang S., Mann A.J., Waldmann J., Weber M., Klindworth A., Otto A., Lange J., Bernhardt J., Reinsch C., Hecker M., Peplies J., Bockelmann F.D., Callies U., Gerdts G., Wichels A., Wiltshire K.H., Glöckner F.O., Schweder T., Amann R. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science (New York, NY) 2012, 336:608-611.
77. Urdea M.S., Warner B.D., Running J.A., Stempien M., Clyne J., Horn T. A comparison of non-radioisotopic hybridization assay methods using fluorescent, chemiluminescent and enzyme labeled synthetic oligodeoxyribonucleotide probes. Nucleic Acids Res. 1988, 16:4937-4956.
78. Wells L.E., Deming J.W. Abundance of bacteria, the Cytophaga-Flavobacterium cluster and Archaea in cold oligotrophic waters and nepheloid layers of the Northwest Passage, Canadian Archipelago. Aquat. Microb. Ecol. 2003, 1-13.
79. Worm J., Gustavson K., Garde K., Borch N.H., Søndergaard M. Functional similarity of attached and free-living bacteria during freshwater phytoplankton blooms. Aquat. Microb. Ecol. 2001, 25:103-111.
80. Yoon J.H., Kang S.J., Oh T.K. Polaribacter dokdonensis sp. nov., isolated from seawater. Int. J. Syst. Evol. Microbiol. 2006, 56:1251-1255.