Water mass and depth determine the distribution and diversity of Rhodobacterales in an Arctic marine system

FEMS Microbiology Ecology

Volumn 84, Issue 3, 2013, Pages 564-576

  Fu, Yunyun ^a   Keats, Kimberley F ^b   Rivkin, Richard B ^b   Lang, Andrew S ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^b MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Baffin Bay; Biogeography; Gene transfer agent; Roseobacter

Indexed keywords

SEA WATER;

ARCTIC ENVIRONMENT; BACTERIUM; BIOGEOGRAPHY; CLONE; COMMUNITY STRUCTURE; GENE TRANSFER; MARINE ECOSYSTEM; MICROBIAL COMMUNITY; PHYLOGENETICS; TAXONOMY; WATER MASS;

ALPHAPROTEOBACTERIA; ARCTIC; ARTICLE; BAY; CLASSIFICATION; DNA SEQUENCE; ECOSYSTEM; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYLOGENY; RHODOBACTERACEAE;

ALPHAPROTEOBACTERIA; ARCTIC REGIONS; BAYS; ECOSYSTEM; PHYLOGENY; RHODOBACTERACEAE; SEAWATER; SEQUENCE ANALYSIS, DNA; WATER MICROBIOLOGY;

ARCTIC OCEAN; BAFFIN BAY [ARCTIC OCEAN];

BACTERIA (MICROORGANISMS); OCTADECABACTER; RHODOBACTERALES; ROSEOBACTER;

EID: 84877715610     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12085     Document Type: Article

References (77)

1. Allgaier M, Uphoff H, Felske A & Wagner-Döbler I (2003) Aerobic anoxygenic photosynthesis in Roseobacter clade bacteria from diverse marine habitats. Appl Environ Microbiol 69: 5051-5059.
2. Baldwin AJ, Moss JA, Pakulski JD, Catala P, Joux F & Jeffrey WH (2005) Microbial diversity in a Pacific Ocean transect from the Arctic to Antarctic circles. Aquat Microb Ecol 41: 91-102.
3. Baltar F, Arístegui J, Gasol J, Hernández-León S & Herndl G (2007) Strong coast-ocean and surface-depth gradients in prokaryotic assemblage structure and activity in a coastal transition zone region. Aquat Microb Ecol 50: 63-74.
4. Biers EJ, Wang K, Pennington C, Belas R, Chen F & Moran MA (2008) Occurrence and expression of gene transfer agent genes in marine bacterioplankton. Appl Environ Microbiol 74: 2933-2939.
5. Bouvier TC & del Giorgio PA (2002) Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol Oceanogr 47: 453-470.
6. Brinkhoff T, Bach G, Heidorn T, Liang L, Schlingloff A & Simon M (2004) Antibiotic production by a Roseobacter clade-affiliated species from the German Wadden Sea and its antagonistic effects on indigenous isolates. Appl Environ Microbiol 70: 2560-2565.
7. Brinkhoff T, Giebel HA & Simon M (2008) Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch Microbiol 189: 531-539.
8. Brinkmeyer R, Knittel K, Jurgens J, Weyland H, Amann R & Helmke E (2003) Diversity and structure of bacterial communities in Arctic versus Antarctic pack ice. Appl Environ Microbiol 69: 6610-6619.
9. Brown MV, Philip GK, Bunge JA, Smith MC, Bissett A, Lauro FM, Fuhrman JA & Donachie SP (2009) Microbial community structure in the North Pacific Ocean. ISME J 3: 1374-1386.
10. Buchan A & González JM (2010) Roseobacter. Handbook of Hydrocarbon and Lipid Microbiology (Timmis KN, ed.), pp. 1335-1343. Springer, Berlin Heidelberg.
11. Buchan A, González JM & Moran MA (2005) Overview of the marine Roseobacter lineage. Appl Environ Microbiol 71: 5665-5677.
12. Buchan A, Hadden M & Suzuki MT (2009) Development and application of quantitative-PCR tools for subgroups of the Roseobacter clade. Appl Environ Microbiol 75: 7542-7547.
13. Cunliffe M (2011) Correlating carbon monoxide oxidation with cox genes in the abundant Marine Roseobacter Clade. ISME J 5: 685-691.
14. Dang H, Li T, Chen M & Huang G (2008) Cross-ocean distribution of Rhodobacterales bacteria as primary surface colonizers in temperate coastal marine waters. Appl Environ Microbiol 74: 52-60.
15. Fu Y, MacLeod DM, Rivkin RB, Chen F, Buchan A & Lang AS (2010) High diversity of Rhodobacterales in the subarctic North Atlantic Ocean and gene transfer agent protein expression in isolated strains. Aquat Microb Ecol 59: 283-293.
16. Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL & Brown JH (2008) A latitudinal diversity gradient in planktonic marine bacteria. P Natl Acad Sci USA 105: 7774-7778.
17. Galand PE, Potvin M, Casamayor EO & Lovejoy C (2010) Hydrography shapes bacterial biogeography of the deep Arctic Ocean. ISME J 4: 564-576.
18. García-Martínez J & Rodríguez-Valera F (2000) Microdiversity of uncultured marine prokaryotes: the SAR11 cluster and the marine Archaea of Group I. Mol Ecol 9: 935-948.
19. Ghiglione J-F, Galand PE, Pommier T et al. (2012) Pole-to-pole biogeography of surface and deep marine bacterial communities. P Natl Acad Sci USA 109: 17633-17638.
20. Giebel HA, Brinkhoff T, Zwisler W, Selje N & Simon M (2009) Distribution of Roseobacter RCA and SAR11 lineages and distinct bacterial communities from the subtropics to the Southern Ocean. Environ Microbiol 11: 2164-2178.
21. Giebel HA, Kalhoefer D, Lemke A, Thole S, Gahl-Janssen R, Simon M & Brinkhoff T (2011) Distribution of Roseobacter RCA and SAR11 lineages in the North Sea and characteristics of an abundant RCA isolate. ISME J 5: 8-19.
22. Gilbert JA, Steele JA, Caporaso JG et al. (2012) Defining seasonal marine microbial community dynamics. ISME J 6: 298-308.
23. González JM & Moran MA (1997) Numerical dominance of a group of marine bacteria in the α-subclass of the class Proteobacteria in coastal seawater. Appl Environ Microbiol 63: 4237-4242.
24. González JM, Simó R, Massana R, Covert JS, Casamayor EO, Pedrós-Alió C & Moran MA (2000) Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appl Environ Microbiol 66: 4237-4246.
25. Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40: 237-264.
26. Gosink JJ, Herwig RP & Staley JT (1997) Octadecabacter arcticus gen. nov., sp. nov., and O. antarcticus, sp. nov., nonpigmented, psychrophilic gas vacuolate bacteria from polar sea ice and water. Syst Appl Microbiol 20: 356-365.
27. Gram L, Grossart HP, Schlingloff A & Kiorboe 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.
28. Green DH, Llewellyn LE, Negri AP, Blackburn SI & Bolch CJS (2004) Phylogenetic and functional diversity of the cultivable bacterial community associated with the paralytic shellfish poisoning dinoflagellate Gymnodinium catenatum. FEMS Microbiol Ecol 47: 345-357.
29. Hale MS, Rivkin RB, Matthews P, Agawin NS & Li WKW (2006) Microbial response to mesoscale iron enrichment in the NE Subarctic Pacific: bacterial dynamics. Deep Sea Res II 53: 2231-2247.
30. Hanson CA, Fuhrman JA, Horner-Devine MC & Martiny JB (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10: 497-506.
31. Hobbie JE, Daley RJ & Jasper S (1977) Use of nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33: 1225-1228.
32. Kristensen DM, Mushegian AR, Dolja VV & Koonin EV (2010) New dimensions of the virus world discovered through metagenomics. Trends Microbiol 18: 11-19.
33. Lang AS & Beatty JT (2007) Importance of widespread gene transfer agent genes in α-proteobacteria. Trends Microbiol 15: 54-62.
34. Lang AS & Beatty JT (2010) Gene transfer agents and defective bacteriophages as sources of extracellular prokaryotic DNA. Extracellular Nucleic Acids (Kikuchi Y & Rykova EY, eds), pp. 15-24. Springer, Heidelberg.
35. Lang AS, Zhaxybayeva O & Beatty JT (2012) Gene transfer agents: phage-like elements of genetic exchange. Nat Rev Microbiol 10: 472-482.
36. Li WKW (1995) Composition of ultraphytoplankton in the central North-Atlantic. Mar Ecol Prog Ser 122: 1-8.
37. Li WKW & Dickie PM (2001) Monitoring phytoplankton, bacterioplankton, and virioplankton in a coastal inlet (Bedford Basin) by flow cytometry. Cytometry 44: 236-246.
38. Lozupone C & Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235.
39. Luo H, Löytynoja A & Moran MA (2012) Genome content of uncultivated marine Roseobacters in the surface ocean. Environ Microbiol 14: 41-51.
40. Marie D, Brussaard CPD, Thyrhaug R, Bratbak G & Vaulot D (1999) Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl Environ Microbiol 65: 45-52.
41. Martens T, Gram L, Grossart HP, Kessler D, Muller R, Simon M, Wenzel SC & Brinkhoff T (2007) Bacteria of the Roseobacter clade show potential for secondary metabolite production. Microb Ecol 54: 31-42.
42. Martiny JB, Bohannan BJ, Brown JH et al. (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4: 102-112.
43. McDaniel LD, Young E, Delaney J, Ruhnau F, Ritchie KB & Paul JH (2010) High frequency of horizontal gene transfer in the oceans. Science 330: 50.
44. McDaniel LD, Young EC, Ritchie KB & Paul JH (2012) Environmental factors influencing Gene Transfer Agent (GTA) mediated transduction in the subtropical ocean. PLoS ONE 7: e43506.
45. Melling H, Gratton Y & Ingram G (2001) Ocean circulation within the North Water polynya of Baffin Bay. Atmosphere-Ocean 39: 301-325.
46. Moran MA, Belas R, Schell MA et al. (2007) Ecological genomics of marine Roseobacters. Appl Environ Microbiol 73: 4559-4569.
47. Morris RM, Rappe MS, Connon SA, Vergin KL, Siebold WA, Carlson CA & Giovannoni SJ (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420: 806-810.
48. Morris RM, Frazar CD & Carlson CA (2012) Basin-scale patterns in the abundance of SAR11 subclades, marine Actinobacteria (OM1), members of the Roseobacter clade and OCS116 in the South Atlantic. Environ Microbiol 14: 1133-1144.
49. Motard-Côté J, Levasseur M, Scarratt MG et al. (2012) Distribution and metabolism of dimethylsulfoniopropionate (DMSP) and phylogenetic affiliation of DMSP-assimilating bacteria in northern Baffin Bay/Lancaster Sound. J Geophys Res - Oceans 117: C00G11.
50. Nemergut DR, Costello EK, Hamady M et al. (2011) Global patterns in the biogeography of bacterial taxa. Environ Microbiol 13: 135-144.
51. Newton RJ, Griffin LE, Bowles KM et al. (2010) Genome characteristics of a generalist marine bacterial lineage. ISME J 4: 784-798.
52. Parsons TR, Maita Y & Lalli CM (1984) A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon, Oxford.
53. Paul JH (2008) Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME J 2: 579-589.
54. Pinhassi J, Winding A, Binnerup SJ, Zweifel UL, Riemann B & Hagström Å (2003) Spatial variability in bacterioplankton community composition at the Skagerrak-Kattegat front. Mar Ecol Prog Ser 255: 1-13.
55. Pommier T, Pinhassi J & Hagström Å (2005) Biogeographic analysis of ribosomal RNA clusters from marine bacterioplankton. Aquat Microb Ecol 41: 79-89.
56. Pommier T, Canback B, Riemann L, Bostrom KH, Simu K, Lundberg P, Tunlid A & Hagstrom A (2007) Global patterns of diversity and community structure in marine bacterioplankton. Mol Ecol 16: 867-880.
57. Saitou N & Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
58. Schattenhofer M, Fuchs BM, Amann R, Zubkov MV, Tarran GA & Pernthaler J (2009) Latitudinal distribution of prokaryotic picoplankton populations in the Atlantic Ocean. Environ Microbiol 11: 2078-2093.
59. Selje N, Simon M & Brinkhoff T (2004) A newly discovered Roseobacter cluster in temperate and polar oceans. Nature 427: 445-448.
60. Seyedsayamdost MR, Case RJ, Kolter R & Clardy J (2011) The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem 3: 331-335.
61. Shannon CE & Weaver W (1949) The Mathematical Theory of Communication. University of Illinois Press, Urbana, IL.
62. Shiba T (1991) Roseobacter litoralis gen. nov., sp. nov., and Roseobacter denitrificans sp. nov., aerobic pink-pigmented bacteria which contain Bacteriochlorophyll a. Syst Appl Microbiol 14: 140-145.
63. Simon M & Azam F (1989) Protein-content and protein-synthesis rates of planktonic marine-bacteria. Mar Ecol Prog Ser 51: 201-213.
64. Sorokin DY (1995) Sulfitobacter pontiacus gen. nov., sp. nov. - a new heterotrophic bacterium from the Black Sea, specialized on sulfite oxidation. Microbiology 64: 295-305.
65. Sperling M, Giebel H, Rink B, Grayek S, Staneva J, Stanev E & Simon M (2012) Differential effects of hydrographic and biogeochemical properties on the SAR11 clade and Roseobacter RCA cluster in the North Sea. Aquat Microb Ecol 67: 25-34.
66. Staley JT & Gosink JJ (1999) Poles apart: biodiversity and biogeography of sea ice bacteria. Annu Rev Microbiol 53: 189-215.
67. Stanton TB (2007) Prophage-like gene transfer agents-Novel mechanisms of gene exchange for Methanococcus, Desulfovibrio, Brachyspira, and Rhodobacter species. Anaerobe 13: 43-49.
68. Tamura K, Nei M & Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. P Natl Acad Sci USA 101: 11030-11035.
69. Tamura K, Dudley J, Nei M & Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
70. Taniguchi A & Hamasaki K (2008) Community structures of actively growing bacteria shift along a north-south transect in the western North Pacific. Environ Microbiol 10: 1007-1017.
71. Thompson JD, Higgins DG & Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
72. Vila-Costa M, Rinta-Kanto JM, Sun S, Sharma S, Poretsky R & Moran MA (2010) Transcriptomic analysis of a marine bacterial community enriched with dimethylsulfoniopropionate. ISME J 4: 1410-1420.
73. Wagner-Döbler I & Biebl H (2006) Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol 60: 255-280.
74. Wagner-Dobler I, Rheims H, Felske A, El-Ghezal A, Flade-Schroder D, Laatsch H, Lang S, Pukall R & Tindall BJ (2004) Oceanibulbus indolifex gen. nov., sp. nov., a North Sea alphaproteobacterium that produces bioactive metabolites. Int J Syst Evol Microbiol 54: 1177-1184.
75. Webster NS, Negri AP, Munro MMHG & Battershill CN (2004) Diverse microbial communities inhabit Antarctic sponges. Environ Microbiol 6: 288-300.
76. Yao D, Buchan A & Suzuki MT (2011) In situ activity of NAC11-7 roseobacters in coastal waters off the Chesapeake Bay based on ftsZ expression. Environ Microbiol 13: 1032-1041.
77. Zhao Y, Wang K, Budinoff C, Buchan A, Lang A, Jiao N & Chen F (2009) Gene transfer agent (GTA) genes reveal diverse and dynamic Roseobacter and Rhodobacter populations in the Chesapeake Bay. ISME J 3: 364-373.