Expansion of Cultured Bacterial Diversity by Large-Scale Dilution-to-Extinction Culturing from a Single Seawater Sample

Microbial Ecology

Volumn 71, Issue 1, 2016, Pages 29-43

  Yang, Seung Jo ^a   Kang, Ilnam ^a   Cho, Jang Cheon ^a  

^a Inha University   (South Korea)

Author keywords

Dilution to extinction; High throughput cultivation; Marine Roseobacter clade; Pyrosequencing; SAR11; Verrucomicrobia

Indexed keywords

BACTERIAL DNA; CULTURE MEDIUM; RNA 16S; SEA WATER;

BACTERIUM; BIODIVERSITY; CLASSIFICATION; CULTURE MEDIUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PACIFIC OCEAN; PHYLOGENY;

BACTERIA; BIODIVERSITY; CULTURE MEDIA; DNA, BACTERIAL; MOLECULAR SEQUENCE DATA; PACIFIC OCEAN; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEAWATER;

EID: 84951567908     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-015-0695-3     Document Type: Article

References (87)

1. Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, Eisen JA, Hoffman JM, Remington K, Beeson K, Tran B, Smith H, Baden-Tillson H, Stewart C, Thorpe J, Freeman J, Andrews-Pfannkoch C, Venter JE, Li K, Kravitz S, Heidelberg JF, Utterback T, Rogers Y-H, Falcón LI, Souza V, Bonilla-Rosso G, Eguiarte LE, Karl DM, Sathyendranath S, Platt T, Bermingham E, Gallardo V, Tamayo-Castillo G, Ferrari MR, Strausberg RL, Nealson K, Friedman R, Frazier M, Venter JC (2007) The sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical pacific. PLoS Biol 5:e77
2. Swan BK, Tupper B, Sczyrba A, Lauro FM, Martinez-Garcia M, González JM, Luo H, Wright JJ, Landry ZC, Hanson NW, Thompson BP, Poulton NJ, Schwientek P, Acinas SG, Giovannoni SJ, Moran MA, Hallam SJ, Cavicchioli R, Woyke T, Stepanauskas R (2013) Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean. Proc Natl Acad Sci U S A 110:11463–11468. doi:10.1073/pnas.1304246110
3. Karl DM, Beversdorf L, Bjorkman KM, Church MJ, Martinez A, Delong EF (2008) Aerobic production of methane in the sea. Nat Geosci 1:473–478
4. Metcalf WW, Griffin BM, Cicchillo RM, Gao J, Janga SC, Cooke HA, Circello BT, Evans BS, Martens-Habbena W, Stahl DA, van der Donk WA (2012) Synthesis of methylphosphonic acid by marine microbes: a source for methane in the aerobic ocean. Science 337:1104–1107. doi:10.1126/science.1219875
5. Carini P, White AE, Campbell EO, Giovannoni SJ (2014) Methane production by phosphate-starved SAR11 chemoheterotrophic marine bacteria. Nat Commun 5:4346. doi:10.1038/ncomms5346
6. Drüppel K, Hensler M, Trautwein K, Koßmehl S, Wöhlbrand L, Schmidt-Hohagen K, Ulbrich M, Bergen N, Meier-Kolthoff JP, Göker M, Klenk H-P, Schomburg D, Rabus R (2014) Pathways and substrate-specific regulation of amino acid degradation in Phaeobacter inhibens DSM 17395 (archetype of the marine Roseobacter clade). Environ Microbiol 16:218–238. doi:10.1111/1462-2920.12276
7. Wiegmann K, Hensler M, Wöhlbrand L, Ulbrich M, Schomburg D, Rabus R (2014) Carbohydrate catabolism in Phaeobacter inhibens DSM 17395, a member of the marine Roseobacter clade. Appl Environ Microbiol 80:4725–4737. doi:10.1128/aem.00719-14doi:10.1128/aem.00719-14
8. Zhao Y, Temperton B, Thrash JC, Schwalbach MS, Vergin KL, Landry ZC, Ellisman M, Deerinck T, Sullivan MB, Giovannoni SJ (2013) Abundant SAR11 viruses in the ocean. Nature 494:357–360. doi:10.1038/nature11921
9. Kang I, Oh H-M, Kang D, Cho J-C (2013) Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans. Proc Natl Acad Sci U S A 110:12343–12348. doi:10.1073/pnas.1219930110
10. Yooseph S, Nealson KH, Rusch DB, McCrow JP, Dupont CL, Kim M, Johnson J, Montgomery R, Ferriera S, Beeson K, Williamson SJ, Tovchigrechko A, Allen AE, Zeigler LA, Sutton G, Eisenstadt E, Rogers Y-H, Friedman R, Frazier M, Venter JC (2010) Genomic and functional adaptation in surface ocean planktonic prokaryotes. Nature 468:60–66
11. Gifford SM, Sharma S, Booth M, Moran MA (2013) Expression patterns reveal niche diversification in a marine microbial assemblage. ISME J 7:281–298. doi:10.1038/ismej.2012.96
12. Rappé MS (2013) Stabilizing the foundation of the house that omics builds: the evolving value of cultured isolates to marine microbiology. Curr Opin Microbiol 16:618–624. doi:10.1016/j.mib.2013.09.009
13. Staley JT, Konopka A (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39:321–346. doi:10.1146/annurev.mi.39.100185.001541
14. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
15. Zengler K, Toledo G, Rappé M, Elkins J, Mathur EJ, Short JM, Keller M (2002) Cultivating the uncultured. Proc Natl Acad Sci U S A 99:15681–15686. doi:10.1073/pnas.252630999
16. Kaeberlein T, Lewis K, Epstein SS (2002) Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296:1127–1129. doi:10.1126/science.1070633
17. Aoi Y, Kinoshita T, Hata T, Ohta H, Obokata H, Tsuneda S (2009) Hollow-fiber membrane chamber as a device for in situ environmental cultivation. Appl Environ Microbiol 75:3826–3833. doi:10.1128/aem.02542-08
18. Steinert G, Whitfield S, Taylor M, Thoms C, Schupp P (2014) Application of diffusion growth chambers for the cultivation of marine sponge-associated bacteria. Mar Biotechnol 16:594–603. doi:10.1007/s10126-014-9575-y
19. Connon SA, Giovannoni SJ (2002) High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new marine isolates. Appl Environ Microbiol 68:3878–3885. doi:10.1128/aem.68.8.3878-3885.2002
20. Tandogan N, Abadian PN, Epstein S, Aoi Y, Goluch ED (2014) Isolation of microorganisms using sub-micrometer constrictions. PLoS ONE 9:e101429. doi:10.1371/journal.pone.0101429
21. Nichols D, Cahoon N, Trakhtenberg EM, Pham L, Mehta A, Belanger A, Kanigan T, Lewis K, Epstein SS (2010) Use of Ichip for high-throughput in situ cultivation of “uncultivable” microbial species. Appl Environ Microbiol 76:2445–2450. doi:10.1128/aem.01754-09
22. Jung D, Seo E-Y, Epstein SS, Joung Y, Han J, Parfenova VV, Belykh OI, Gladkikh AS, Ahn TS (2014) Application of a new cultivation technology, I-tip, for studying microbial diversity in freshwater sponges of lake Baikal, Russia. FEMS Microbiol Ecol 90:417–423. doi:10.1111/1574-6941.12399
23. Rappe MS, Connon SA, Vergin KL, Giovannoni SJ (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418:630–633
24. Cho J-C, Giovannoni SJ (2004) Cultivation and growth characteristics of a diverse group of oligotrophic marine Gammaproteobacteria. Appl Environ Microbiol 70:432–440. doi:10.1128/aem.70.1.432-440.2004
25. Cho J-C, Vergin KL, Morris RM, Giovannoni SJ (2004) Lentisphaera araneosa gen. nov., sp. nov, a transparent exopolymer producing marine bacterium, and the description of a novel bacterial phylum, Lentisphaerae. Environ Microbiol 6:611–621. doi:10.1111/j.1462-2920.2004.00614.x
26. Giovannoni SJ, Hayakawa DH, Tripp HJ, Stingl U, Givan SA, Cho J-C, Oh H-M, Kitner JB, Vergin KL, Rappé MS (2008) The small genome of an abundant coastal ocean methylotroph. Environ Microbiol 10:1771–1782. doi:10.1111/j.1462-2920.2008.01598.x
27. Grote J, Bayindirli C, Bergauer K, De Moraes PC, Chen H, D’Ambrosio L, Edwards B, Fernández-Gómez B, Hamisi M, Logares R, Nguyen D, Rii Y, Saeck E, Schutte C, Widner B, Church M, Steward G, Karl D, DeLong E, Eppley J, Schuster SC, Kyrpides N, Rappe M (2011) Complete genome sequence of strain HIMB100, a cultured representative of the SAR116 clade of marine Alphaproteobacteria. Stand Genomic Sci 5:269–278
28. Marshall KT, Morris RM (2012) Isolation of an aerobic sulfur oxidizer from the SUP05/Arctic96BD-19 clade. ISME J 7:452–455. doi:10.1038/ismej.2012.78
29. 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
30. Song J, Oh H-M, Cho J-C (2009) Improved culturability of SAR11 strains in dilution-to-extinction culturing from the East Sea, West Pacific Ocean. FEMS Microbiol Lett 295:141–147
31. Lane D (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175
32. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In: Nucleic acids symposium series, Vol. 41, pp 95-98
33. Giovannoni SJ, Rappé MS, Vergin KL, Adair NL (1996) 16S rRNA genes reveal stratified open ocean bacterioplankton populations related to the green non-sulfur bacteria. Proc Natl Acad Sci U S A 93:7979–7984
34. Turner S, Pryer KM, Miao VPW, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327–338. doi:10.1111/j.1550-7408.1999.tb04612.x
35. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/aem.01541-09
36. Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS ONE 6:e27310. doi:10.1371/journal.pone.0027310
37. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Buchner A, Yadhukumar, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüßmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371
38. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5–W9. doi:10.1093/nar/gkn201
39. Kim O-S, Cho Y-J, Lee K, Yoon S-H, Kim M, Na H, Park S-C, Jeon YS, Lee J-H, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721. doi:10.1099/ijs.0.038075-0
40. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121
41. 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
42. Vartoukian SR, Palmer RM, Wade WG (2010) Strategies for culture of ‘unculturable’ bacteria. FEMS Microbiol Lett 309:1–7. doi:10.1111/j.1574-6968.2010.02000.x
43. 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
44. Grote J, Thrash JC, Huggett MJ, Landry ZC, Carini P, Giovannoni SJ, Rappé MS (2012) Streamlining and core genome conservation among highly divergent members of the SAR11 clade. mBio 3:e00252-12. doi:10.1128/mBio.00252-12
45. Thrash JC, Boyd A, Huggett MJ, Grote J, Carini P, Yoder RJ, Robbertse B, Spatafora JW, Rappe MS, Giovannoni SJ (2011) Phylogenomic evidence for a common ancestor of mitochondria and the SAR11 clade. Sci Rep 1:13
46. Viklund J, Martijn J, Ettema TJG, Andersson SGE (2013) Comparative and phylogenomic evidence that the alphaproteobacterium HIMB59 is not a member of the oceanic SAR11 Clade. PLoS ONE 8:e78858. doi:10.1371/journal.pone.0078858
47. Luo H (2015) Evolutionary origin of a streamlined marine bacterioplankton lineage. ISME J 9:1423–1433. doi:10.1038/ismej.2014.227
48. Buchan A, González JM, Moran MA (2005) Overview of the marine Roseobacter lineage. Appl Environ Microbiol 71:5665–5677. doi:10.1128/aem.71.10.5665-5677.2005
49. Suzuki MT, Preston CM, Béjà O, de la Torre JR, Steward GF, DeLong EF (2004) Phylogenetic screening of ribosomal RNA gene-containing clones in bacterial artificial chromosome (BAC) libraries from different depths in Monterey Bay. Microb Ecol 48:473–488. doi:10.1007/s00248-004-0213-5
50. Obernosterer I, Catala P, Lebaron P, West NJ (2011) Distinct bacterial groups contribute to carbon cycling during a naturally iron fertilized phytoplankton bloom in the Southern Ocean. Limnol Oceanogr 56:2391–2401
51. Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, Kassabgy M, Huang S, Mann AJ, Waldmann J, Weber M, Klindworth A, Otto A, Lange J, Bernhardt J, Reinsch C, Hecker M, Peplies J, Bockelmann FD, Callies U, Gerdts G, Wichels A, Wiltshire KH, Glöckner FO, Schweder T, Amann R (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336:608–611. doi:10.1126/science.1218344
52. Giovannoni SJ, Vergin KL (2012) Seasonality in ocean microbial communities. Science 335:671–676. doi:10.1126/science.1198078
53. Oh H-M, Kwon KK, Kang I, Kang SG, Lee J-H, Kim S-J, Cho J-C (2010) Complete genome sequence of “Candidatus puniceispirillum marinum” IMCC1322, a representative of the SAR116 clade in the Alphaproteobacteria. J Bacteriol 192:3240–3241. doi:10.1128/jb.00347-10
54. Treusch AH, Vergin KL, Finlay LA, Donatz MG, Burton RM, Carlson CA, Giovannoni SJ (2009) Seasonality and vertical structure of microbial communities in an ocean gyre. ISME J 3:1148–1163
55. Jimenez-Infante F, Ngugi DK, Alam I, Rashid M, Baalawi W, Kamau AA, Bajic VB, Stingl U (2014) Genomic differentiation among two strains of the PS1 clade isolated from geographically separated marine habitats. FEMS Microbiol Ecol 89:181–197. doi:10.1111/1574-6941.12348
56. Morris RM, Vergin KL, Cho JC, Rappé MS, Carlson CA, Giovannoni SJ (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
57. Iverson V, Morris RM, Frazar CD, Berthiaume CT, Morales RL, Armbrust EV (2012) Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota. Science 335:587–590. doi:10.1126/science.1212665
58. Yang S-J, Kang I, Cho J-C (2012) Genome sequence of strain IMCC14465, isolated from the East Sea, belonging to the PS1 clade of Alphaproteobacteria. J Bacteriol 194:6952–6953. doi:10.1128/jb.01888-12
59. Stingl U, Desiderio RA, Cho J-C, Vergin KL, Giovannoni SJ (2007) The SAR92 clade: an abundant coastal clade of culturable marine bacteria possessing proteorhodopsin. Appl Environ Microbiol 73:2290–2296. doi:10.1128/aem.02559-06
60. Yan S, Fuchs BM, Lenk S, Harder J, Wulf J, Jiao N-Z, Amann R (2009) Biogeography and phylogeny of the NOR5/OM60 clade of Gammaproteobacteria. Syst Appl Microbiol 32:124–139
61. Huggett MJ, Rappé MS (2012) Genome sequence of strain HIMB55, a novel marine gammaproteobacterium of the OM60/NOR5 clade. J Bacteriol 194:2393–2394. doi:10.1128/jb.00171-12
62. Pham VD, Konstantinidis KT, Palden T, DeLong EF (2008) Phylogenetic analyses of ribosomal DNA-containing bacterioplankton genome fragments from a 4000 m vertical profile in the North Pacific Subtropical Gyre. Environ Microbiol 10:2313–2330. doi:10.1111/j.1462-2920.2008.01657.x
63. Wilkins D, Yau S, Williams TJ, Allen MA, Brown MV, DeMaere MZ, Lauro FM, Cavicchioli R (2013) Key microbial drivers in Antarctic aquatic environments. FEMS Microbiol Rev 37:303–335. doi:10.1111/1574-6976.12007
64. Nelson CE, Carlson CA (2012) Tracking differential incorporation of dissolved organic carbon types among diverse lineages of Sargasso sea bacterioplankton. Environ Microbiol 14:1500–1516. doi:10.1111/j.1462-2920.2012.02738.x
65. Wemheuer B, Güllert S, Billerbeck S, Giebel H-A, Voget S, Simon M, Daniel R (2014) Impact of a phytoplankton bloom on the diversity of the active bacterial community in the southern North Sea as revealed by metatranscriptomic approaches. FEMS Microbiol Ecol 87:378–389. doi:10.1111/1574-6941.12230
66. Sowell SM, Abraham PE, Shah M, Verberkmoes NC, Smith DP, Barofsky DF, Giovannoni SJ (2011) Environmental proteomics of microbial plankton in a highly productive coastal upwelling system. ISME J 5:856–865
67. Spring S, Riedel T, Sproer C, Yan S, Harder J, Fuchs B (2013) Taxonomy and evolution of bacteriochlorophyll a-containing members of the OM60/NOR5 clade of marine gammaproteobacteria: description of Luminiphilus syltensis gen. nov., sp. nov., reclassification of Haliea rubra as Pseudohaliea rubra gen. nov., comb. nov., and emendation of Chromatocurvus halotolerans. BMC Microbiol 13:118
68. Cho J-C, Stapels MD, Morris RM, Vergin KL, Schwalbach MS, Givan SA, Barofsky DF, Giovannoni SJ (2007) Polyphyletic photosynthetic reaction centre genes in oligotrophic marine Gammaproteobacteria. Environ Microbiol 9:1456–1463. doi:10.1111/j.1462-2920.2007.01264.x
69. Jang Y, Oh H-M, Kang I, Lee K, Yang S-J, Cho J-C (2011) Genome sequence of strain IMCC3088, a proteorhodopsin-containing marine bacterium belonging to the OM60/NOR5 clade. J Bacteriol 193:3415–3416. doi:10.1128/jb.05111-11
70. Spring S, Scheuner C, Göker M, Klenk H-P (2015) A taxonomic framework for emerging groups of ecologically important marine gammaproteobacteria based on the reconstruction of evolutionary relationships using genome-scale data. Front Microbiol 9(6):281. doi:10.3389/fmicb.2015.00281
71. Kang I, Kang D, Oh H-M, Kim H, Kim H-J, Kang T-W, Kim S-Y, Cho J-C (2011) Genome sequence of strain IMCC2047, a novel marine member of the Gammaproteobacteria. J Bacteriol 193:3688–3689. doi:10.1128/jb.05226-11
72. Rappé MS, Kemp PF, Giovannoni SJ (1997) Phylogenetic diversity of marine coastal picoplankton 16s rRNA genes cloned from the continental shelf off Cape Hatteras, North Carolina. Limnol Oceanogr 42:811–826
73. Huggett M, Hayakawa D, Rappe M (2012) Genome sequence of strain HIMB624, a cultured representative from the OM43 clade of marine Betaproteobacteria. Stand Genomic Sci 6:11–20
74. Freitas S, Hatosy S, Fuhrman JA, Huse SM, Mark Welch DB, Sogin ML, Martiny AC (2012) Global distribution and diversity of marine Verrucomicrobia. ISME J 6:1499–1505
75. Choo Y-J, Lee K, Song J, Cho J-C (2007) Puniceicoccus vermicola gen. nov., sp. nov., a novel marine bacterium, and description of Puniceicoccaceae fam. nov., Puniceicoccales ord. nov., Opitutaceae fam. nov., Opitutales ord. nov. and Opitutae classis nov. In the phylum ‘Verrucomicrobia’. Int J Syst Evol Microbiol 57:532–537. doi:10.1099/ijs.0.64616-0
76. Yoon J, Yasumoto-Hirose M, Katsuta A, Sekiguchi H, Matsuda S, Kasai H, Yokota A (2007) Coraliomargarita akajimensis gen. nov., sp. nov., a novel member of the phylum ‘Verrucomicrobia’ isolated from seawater in Japan. Int J Syst Evol Microbiol 57:959–963. doi:10.1099/ijs.0.64755-0
77. Kant R, van Passel MWJ, Sangwan P, Palva A, Lucas S, Copeland A, Lapidus A, Glavina del Rio T, Dalin E, Tice H, Bruce D, Goodwin L, Pitluck S, Chertkov O, Larimer FW, Land ML, Hauser L, Brettin TS, Detter JC, Han S, de Vos WM, Janssen PH, Smidt H (2011) Genome sequence of “Pedosphaera parvula” Ellin514, an aerobic verrucomicrobial isolate from pasture soil. J Bacteriol 193:2900–2901. doi:10.1128/jb.00299-11
78. Martinez-Garcia M, Brazel DM, Swan BK, Arnosti C, Chain PSG, Reitenga KG, Xie G, Poulton NJ, Gomez ML, Masland DED, Thompson B, Bellows WK, Ziervogel K, Lo C-C, Ahmed S, Gleasner CD, Detter CJ, Stepanauskas R (2012) Capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of Verrucomicrobia. PLoS ONE 7:e35314. doi:10.1371/journal.pone.0035314
79. Choi A, Yang S-J, Rhee K-H, Cho J-C (2013) Lentisphaera marina sp. nov., and emended description of the genus Lentisphaera. Int J Syst Evol Microbiol 63:1540–1544. doi:10.1099/ijs.0.046433-0
80. Yilmaz P, Iversen MH, Hankeln W, Kottmann R, Quast C, Glöckner FO (2012) Ecological structuring of bacterial and archaeal taxa in surface ocean waters. FEMS Microbiol Ecol 81:373–385. doi:10.1111/j.1574-6941.2012.01357.x
81. Zinger L, Boetius A, Ramette A (2014) Bacterial taxa–area and distance–decay relationships in marine environments. Mol Ecol 23:954–964. doi:10.1111/mec.12640
82. Cottrell MT, Kirchman DL (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. doi:10.1128/aem.66.4.1692-1697.2000
83. Fernandez-Gomez B, Richter M, Schuler M, Pinhassi J, Acinas SG, Gonzalez JM, Pedros-Alio C (2013) Ecology of marine Bacteroidetes: a comparative genomics approach. ISME J 7:1026–1037. doi:10.1038/ismej.2012.169
84. 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. doi:10.1111/j.1462-2920.2011.02694.x
85. Halsey KH, Carter AE, Giovannoni SJ (2011) Synergistic metabolism of a broad range of C1 compounds in the marine methylotrophic bacterium HTCC2181. Environ Microbiol 14:630–640. doi:10.1111/j.1462-2920.2011.02605.x
86. Sosa OA, Gifford SM, Repeta DJ, DeLong EF (2015) High molecular weight dissolved organic matter enrichment selects for methylotrophs in dilution to extinction cultures. ISME J. doi:10.1038/ismej.2015.68
87. Newton RJ, Griffin LE, Bowles KM, Meile C, Gifford S, Givens CE, Howard EC, King E, Oakley CA, Reisch CR, Rinta-Kanto JM, Sharma S, Sun S, Varaljay V, Vila-Costa M, Westrich JR, Moran MA (2010) Genome characteristics of a generalist marine bacterial lineage. ISME J 4:784–798