Combined Analyses of the ITS Loci and the Corresponding 16S rRNA Genes Reveal High Micro- and Macrodiversity of SAR11 Populations in the Red Sea

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Ngugi, David Kamanda ^a   Stingl, Ulrich ^a  

^a KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

DISSOLVED OXYGEN; DNA FRAGMENT; INTERNAL TRANSCRIBED SPACER; RNA 16S; SEA WATER;

ARTICLE; CLADISTICS; COMMUNITY STRUCTURE; CONTROLLED STUDY; DNA SEQUENCE; ECOTYPE; ENVIRONMENTAL TEMPERATURE; GENE LOCUS; GENETIC ANALYSIS; INDIAN OCEAN; MARINE BACTERIUM; MARINE ENVIRONMENT; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT AVAILABILITY; OXYGEN CONCENTRATION; POPULATION ABUNDANCE; POPULATION DYNAMICS; RESOURCE PARTITIONING; RNA GENE; SAR11 BACTERIUM; SEASONAL VARIATION; UNINDEXED SEQUENCE;

ALPHAPROTEOBACTERIA; BASE SEQUENCE; BIODIVERSITY; DNA, BACTERIAL; DNA, INTERGENIC; ECOSYSTEM; GENETIC LOCI; INDIAN OCEAN; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANKTON; RNA, RIBOSOMAL, 16S; SALINITY; TEMPERATURE;

BACTERIA (MICROORGANISMS); PROKARYOTA;

EID: 84869756836     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050274     Document Type: Article

References (93)

1. Morris RM, Rappé MS, Connon SA, Vergin KL, Siebold WA, et al. (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420: 806-810.
2. Carlson CA, Morris R, Parsons R, Treusch AH, Giovannoni SJ, et al. (2008) Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea. ISME J 3: 283-295.
3. Eiler A, Hayakawa DH, Church MJ, Karl DM, Rappé MS, (2009) Dynamics of the SAR11 bacterioplankton lineage in relation to environmental conditions in the oligotrophic North Pacific subtropical gyre. Environ Microbiol 11: 2291-2300.
4. Rappé MS, Connon SA, Vergin KL, Giovannoni SJ, (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418: 630-633.
5. Malmstrom R, Kiene R, Cottrell M, Kirchman D, (2004) Contribution of SAR11 bacteria to dissolved dimethylsulfoniopropionate and amino acid uptake in the North Atlantic Ocean. Appl Environ Microbiol 70: 4129-4135.
6. Tripp HJ, Kitner JB, Schwalbach MS, Dacey JWH, Wilhelm LJ, et al. (2008) SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 452: 741-744.
7. Sun J, Steindler L, Thrash JC, Harsely KH, Smith DP, et al. (2011) One carbon metabolism in SAR11 pelagic marine Bacteria. PLoS ONE 6: e23973.
8. Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL, et al. (2005) Genome Streamlining in a cosmopolitan oceanic bacterium. Science 309: 1242-1245.
9. Oh H-M, Kang I, Lee K, Jang Y, Lim S-I, et al. (2011) Complete genome sequence of strain IMCC9063, belonging to SAR11 subgroup 3, isolated from the Arctic Ocean. J Bacteriol 193: 3379-3380.
10. Sowell SM, Norbeck AD, Lipton MS, Nicora CD, Callister SJ, et al. (2008) Proteomic analysis of stationary phase in the marine bacterium "Candidatus Pelagibacter ubique". Appl Environ Microbiol 74: 4091-4100.
11. Schwalbach MS, Tripp HJ, Steindler L, Smith DP, Giovannoni SJ, (2010) The presence of the glycolysis operon in SAR11 genomes is positively correlated with ocean productivity. Environ Microbiol 12: 490-500.
12. Rappé MS, Giovannoni SJ, (2003) The uncultured microbial majority. Annu Rev Microbiol 57: 369-394.
13. Logares R, Brate J, Heinrich F, Shalchian-Tabrizi K, Bertilsson S, (2010) Infrequent transitions between saline and fresh waters in one of the most abundant microbial lineages (SAR11). Mol Biol Evol 27: 347-357.
14. 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.
15. Brown MV, Schwalbach MS, Hewson I, Fuhrman JA, (2005) Coupling 16S-ITS rDNA clone libraries and automated ribosomal intergenic spacer analysis to show marine microbial diversity: development and application to a time series. Environ Microbiol 7: 1466-1479.
16. Giovannoni SJ, Bibbs L, Cho J-C, Stapels MD, Desiderio R, et al. (2005) Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438: 82-85.
17. Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, et al. (2007) The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol 5: e77.
18. Stingl U, Tripp HJ, Giovannoni SJ, (2007) Improvements of high-throughput culturing yielded novel SAR11 strains and other abundant marine bacteria from the Oregon coast and the Bermuda Atlantic Time Series study site. ISME J 1: 361-371.
19. Vergin KL, Tripp HJ, Wilhelm LJ, Denver DR, Rappé MS, et al. (2007) High intraspecific recombination rate in a native population of Candidatus pelagibacter ubique (SAR11). Environ Microbiol 9: 2430-2440.
20. Wilhelm LJ, Tripp HJ, Givan SA, Smith DP, Giovannoni SJ, (2007) Natural variation in SAR11 marine bacterioplankton genomes inferred from metagenomic data. Biol Direct 2: 27.
21. Viklund J, Ettema TJG, Andersson SGE, (2012) Independent genome reduction and phylogenetic reclassification of the oceanic SAR11 clade. Mol Biol Evol 29: 599-615.
22. Pommier T, Canback B, Riemann L, Bostrom KH, Simu K, et al. (2007) Global patterns of diversity and community structure in marine bacterioplankton. Mol Ecol 16: 867-880.
23. Brown M, Fuhrman J, (2005) Marine bacterial microdiversity as revealed by internal transcribed spacer analysis. Aquat Microb Ecol 41: 15-23.
24. Brown MV, Lauro FM, Demaere MZ, Muir L, Wilkins D, et al. (2012) Global biogeography of SAR11 marine bacteria. Mol Syst Biol 8: 595.
25. Field KG, Gordon D, Wright T, Rappé M, Urback E, et al. (1997) Diversity and depth-specific distribution of SAR11 cluster rRNA genes from marine planktonic bacteria. Appl Environ Microbiol 63: 63-70.
26. Morris R, Vergin K, Cho J, Rappe M, Carlson C, et al. (2005) Temporal and spatial response of bacterioplankton lineages to annual convective overturn at the Bermuda Atlantic Time-series Study site. Limnol Oceanogr 50: 1687-1696.
27. Lami R, Cottrell MT, Campbell BJ, Kirchman DL, (2009) Light-dependent growth and proteorhodopsin expression by Flavobacteria and SAR11 in experiments with Delaware coastal waters. Environ Microbiol 11: 3201-3209.
28. Salcher MM, Pernthaler J, Posch T, (2011) Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria 'that rule the waves' (LD12). ISME J 5: 1242-1252.
29. Martiny AC, Huang Y, Li W (2011) Adaptation to nutrient availability in marine microorganisms by gene gain and loss. In: de Bruijin FJ, editor. Handbook of Molecular Microbial Ecology II: Metagenomics in Different Habitats. John Wiley and Sons. 269-276.
30. Giovannoni SJ, Vergin KL, (2012) Seasonality in ocean microbial communities. Science 335: 671-676.
31. Cohan FM, (2002) What are bacterial species? Annu Rev Microbiol 56: 457-487.
32. Rocap G, Distel DL, Waterbury JB, Chisholm SW, (2002) Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 68: 1180-1191.
33. Ngugi DK, Antunes A, Brune A, Stingl U, (2011) Biogeography of pelagic bacterioplankton across an antagonistic temperature-salinity gradient in the Red Sea. Mol Ecol 21: 388-405.
34. DuRand M, Olson R, Chisholm S, (2001) Phytoplankton population dynamics at the Bermuda Atlantic Time-series station in the Sargasso Sea. Deep-Sea Res Pt Ii 48: 1983-2003.
35. Manasrah R, Badran M, Lass H, Fennel W, (2004) Circulation and winter deep-water formation in the northern Red Sea. Oceanologia 46: 5-23.
36. Qian P-Y, Wang Y, Lee OO, Lau SCK, Yang J, et al. (2011) Vertical stratification of microbial communities in the Red Sea revealed by 16S rDNA pyrosequencing. ISME J 5: 507-518.
37. Stambler N, (2005) Bio-optical properties of the northern Red Sea and the Gulf of Eilat (Aqaba) during winter 1999. J Sea Res 54: 186-203.
38. Morcos SA (1970) Physical and chemical oceanography of the Red Sea. Oceanography and Marine Biology: An Annual Review 8.
39. Edwards A (1987) Climate and Oceanography. In: Alasdair EJ, Stephen HM, editors. Key Environments: Red Sea. Headington Hill Hall, UK.: Pergamon Books Ltd. 45-68.
40. Zaballos M, Lopez-Lopez A, Ovreas L, Bartual S, D'Auria G, et al. (2006) Comparison of prokaryotic diversity at offshore oceanic locations reveals a different microbiota in the Mediterranean Sea. FEMS Microbiol Ecol 56: 389-405.
41. Danovaro R, (2010) Company JB, Corinaldesi C, D'Onghia G, Galil B, et al (2010) Deep-sea biodiversity in the Mediterranean Sea: the known, the unknown, and the unknowable. PLoS ONE 5: e11832.
42. Cember R, (1988) On the sources, formation, and circulation of Red-Sea deep-water. J Geophys Res-Oceans 93: 8175-8191.
43. Stein M, Almogi-Labin A, Goldstein SL, Hemleben C, Starinsky A, (2007) Late Quaternary changes in desert dust inputs to the Red Sea and Gulf of Aden from 87Sr/86Sr ratios in deep-sea cores. Earth and Planetary Science Letters 261: 104-119.
44. Grote J, Thrash JC, Huggett MJ, Landry ZC, Carini P, et al. (2012) Streamlining and core genome conservation among highly divergent members of the SAR11 clade. MBio 3(5): e00252-12 doi:10.1128/mBio.00252-12.
45. Zwart G, Hiorns WD, Methé BA, van Agterveld MP, Huismans R, et al. (1998) Nearly identical 16S rRNA sequences recovered from lakes in North America and Europe indicate the existence of clades of globally distributed freshwater bacteria. Syst Appl Microbiol 21: 546-556.
46. Glöckner FO, Zaichikov E, Belkova N, Denissova L, Pernthaler J, et al. (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of actinobacteria. Appl Environ Microbiol 66: 5053-5065.
47. Suzuki MT, Béjà O, Taylor LT, Delong EF, (2001) Phylogenetic analysis of ribosomal RNA operons from uncultivated coastal marine bacterioplankton. Environ Microbiol 3: 323-331.
48. Thrash JC, Boyd A, Huggett MJ, Grote J, Carini P, et al. (2011) Phylogenomic evidence for a common ancestor of mitochondria and the SAR11 clade. Sci Rep 1: 13.
49. Gilbert JA, Mühling M, Joint I, (2008) A rare SAR11 fosmid clone confirming genetic variability in the "Candidatus Pelagibacter ubique" genome. ISME J 2: 790-793.
50. Johnson ZI, (2006) Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311: 1737-1740.
51. Follows MJ, Dutkiewicz S, Grant S, Chisholm SW, (2007) Emergent biogeography of microbial communities in a model ocean. Science 315: 1843-1846.
52. Trommer G, Siccha M, van der Meer MTJ, Schouten S, Damsté JSS, et al. (2009) Distribution of Crenarchaeota tetraether membrane lipids in surface sediments from the Red Sea. Organic Geochemistry 40: 724-731.
53. Haverkamp THA, Schouten D, Doeleman M, Wollenzien U, Huisman J, et al. (2008) Colorful microdiversity of Synechococcus strains (picocyanobacteria) isolated from the Baltic Sea. ISME J 3: 397-408.
54. Kirchman D, Elifantz H, Dittel A, Malmstrom R, Cottrell M, (2007) Standing stocks and activity of Archaea and Bacteria in the western Arctic Ocean. Limnol Oceanography 52: 495-507.
55. De Corte D, Yokokawa T, Varela MM, Agogue H, Herndl GJ, (2009) Spatial distribution of Bacteria and Archaea and amoA gene copy numbers throughout the water column of the Eastern Mediterranean Sea. ISME J 3: 147-158.
56. Hu A, Jiao N, Zhang R, Yang Z, (2011) Niche partitioning of Marine Group I Crenarchaeota in the euphotic and upper mesopelagic zones of the East China Sea. Appl Environ Microbiol 77: 7469-7478.
57. Fraser C, Hanage WP, Spratt BG, (2007) Recombination and the nature of bacterial speciation. Science 315: 476-480.
58. Sohm JA, Webb EA, Capone DG, (2011) Emerging patterns of marine nitrogen fixation. Nat Rev Micro 9: 499-508.
59. Clarke A, (2003) Costs and consequences of evolutionary temperature adaptation. Trends in Ecol Evol 18: 573-581.
60. Paytan A, Mackey KRM, Chen Y, Lima ID, Doney SC, et al. (2009) Toxicity of atmospheric aerosols on marine phytoplankton. Proc Natl Acad Sci USA 106: 4601-4605.
61. Wu J, (2001) Soluble and colloidal Iron in the oligotrophic North Atlantic and North Pacific. Science 293: 847-849.
62. Wu J, (2000) Phosphate Depletion in the Western North Atlantic Ocean. Science 289: 759-762.
63. Buesseler KO, (2004) The effects of iron fertilization on carbon sequestration in the Southern Ocean. Science 304: 414-417.
64. Mackey KRM, Rivlin T, Grossman AR, Post AF, Paytan A, (2009) Picophytoplankton responses to changing nutrient and light regimes during a bloom. Marine Biol 156: 1531-1546.
65. Rodriguez-Valera F, Martin-Cuadrado A-B, Rodriguez-Brito B, Pasić L, Thingstad TF, et al. (2009) Explaining microbial population genomics through phage predation. Nat Rev Micro 7: 828-836.
66. Moigis AG, (2000) Photosynthetic rates in the surface waters of the Red Sea: the radiocarbon versus the non-isotopic dilution method. J of Plankton Res 22: 713-727.
67. Boelen P, Post AF, Veldhuis MJW, Buma AGJ, (2002) Diel patterns of UVBR-induced DNA damage in picoplankton size fractions from the Gulf of Aqaba, Red Sea. Microb Ecol 44: 164-174.
68. Alonso-Sáez L, Gasol JM, Lefort T, Hofer J, Sommaruga R, (2006) Effect of natural sunlight on bacterial activity and differential sensitivity of natural bacterioplankton groups in northwestern Mediterranean coastal waters. Appl Environ Microbiol 72: 5806-5813.
69. Straza TRA, Kirchman DL, (2011) Single-cell response of bacterial groups to light and other environmental factors in the Delaware Bay, USA. Aquat Microb Ecol 62: 267-U281.
70. Ruiz-González C, Lefort T, Galí M, Montserrat Sala M, Sommaruga R, et al. (2012) Seasonal patterns in the sunlight sensitivity of bacterioplankton from Mediterranean surface coastal waters. FEMS Microbiol Ecol 79: 661-674.
71. Béjà O, Aravind L, Koonin EV, Suzuki MT, Hadd A, et al. (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289: 1902-1906.
72. Sabehi G, Kirkup BC, Rozenberg M, Stambler N, Polz MF, et al. (2007) Adaptation and spectral tuning in divergent marine proteorhodopsins from the eastern Mediterranean and the Sargasso Seas. ISME J 1: 48-55.
73. Dishon G, Dubinsky Z, Caras T, Rahav E, Bar-Zeev E, et al. (2012) Optical habitats of ultraphytoplankton groups in the Gulf of Eilat (Aqaba), Northern Red Sea. International J Remote Sensing 33: 2683-2705.
74. Falcón LI, Noguez AM, Espinosa-Asuar L, Eguiarte LE, Souza V, (2008) Evidence of biogeography in surface ocean bacterioplankton assemblages. Marine Genomics 1: 55-61.
75. Yooseph S, Nealson KH, Rusch DB, McCrow JP, Dupont CL, et al. (2010) Genomic and functional adaptation in surface ocean planktonic prokaryotes. Nature 468: 60-66.
76. Dupont CL, Rusch DB, Yooseph S, Lombardo M-J, Alexander Richter R, et al. (2011) Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage. ISME J.
77. Cavender-Bares K, Karl D, Chisholm S, (2001) Nutrient gradients in the western North Atlantic Ocean: Relationship to microbial community structure and comparison to patterns in the Pacific Ocean. Deep Sea Research Part I: Oceanographic Research Papers 48: 2373-2395.
78. Farías L, Paulmier A, Gallegos M, (2007) Nitrous oxide and N-nutrient cycling in the oxygen minimum zone off northern Chile. Deep Sea Research Part I: Oceanographic Research Papers 54: 164-180.
79. Stewart FJ, Sharma AK, Bryant JA, Eppley JM, DeLong EF, (2011) Community transcriptomics reveals universal patterns of protein sequence conservation in natural microbial communities. Genome Biol 12: R26.
80. Coleman ML, Chisholm SW, (2010) Ecosystem-specific selection pressures revealed through comparative population genomics. Proc Natl Acad Sci USA 107: 18634-18639.
81. Martiny AC, Huang Y, Li W, (2009) Occurrence of phosphate acquisition genes in Prochlorococcus cells from different ocean regions. Environ Microbiol 11: 1340-1347.
82. Sowell SM, Wilhelm LJ, Norbeck AD, Lipton MS, Nicora CD, et al. (2009) Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea. ISME J 3: 93-105.
83. Campbell L, Vaulot D, (1993) Photosynthetic picoplankton community structure in the subtropical North Pacific-Ocean near Hawaii (Station Aloha). Deep Sea Research Part I: Oceanographic Research Papers 40: 2043-2060.
84. Galán A, Molina V, Thamdrup B, Woebken D, Lavik G, et al. (2009) Anammox bacteria and the anaerobic oxidation of ammonium in the oxygen minimum zone off northern Chile. Deep-Sea Res Pt Ii 56: 1021-1031.
85. Bryant JA, Stewart FJ, Epply JM, DeLong EF (2012) Microbial community phylogenetic and trait diversity declines with depth in a marine oxygen minimum zone. Ecology: 120131072157003.
86. Revsbech NP, Larsen LH, Gundersen J, Dalsgaard T, Ulloa O, et al. (2009) Determination of ultra-low oxygen concentrations in oxygen minimum zones by the STOX sensor. Limnol Oceangr Methods 7: 371-381.
87. Stewart FJ, Ulloa O, DeLong EF, (2012) Microbial metatranscriptomics in a permanent marine oxygen minimum zone. Environ Microbiol 14: 23-40.
88. Sun J, Steindler L, Thrash JC, Halsey KH, Smith DP, et al. (2011) One carbon metabolism in SAR11 pelagic marine Bacteria. PLoS ONE 6: e23973.
89. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
90. Faith DP, (1992) Systematics and conservation: on predicting the feature diversity of subsets of taxa. Cladistics 8: 361-373.
91. Lozupone C, Knight R, (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235.
92. Ludwig W, Strunk O, Westram R, Richter L, Meier H, et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
93. Martin AP, (2002) Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl Environ Microbiol 68: 3673-3682.