Marine Biology

, Volume 156, Issue 3, pp 425–437 | Cite as

Genetic diversity of aerobic anoxygenic photosynthetic bacteria in open ocean surface waters and upper twilight zones

  • Yonghui Zeng
  • Wei Shen
  • Nianzhi JiaoEmail author
Original Paper


Aerobic anoxygenic phototrophic bacteria (AAPB) represent a widespread mixotrophic bacterial group in marine ecosystems. Here we investigated AAPB genetic diversity in the surface waters and upper twilight zones of the central Pacific, Atlantic, and Indian oceans by amplifying an AAPB marker gene (pufM, encoding photosynthetic reaction center small subunit) directly from bacterioplankton community DNA. Phylogenetic and statistical analysis of 267 pufM partial sequences in six clone libraries revealed a high diversity pattern in open ocean AAPB communities. Various AAPB subgroups belonging to Alpha- and Gamma-proteobacteria were found in both surface and upper twilight zone waters. In most samples, subgroups in which no pure culture was isolated as yet were predominant. By sampling a wide size range of bacterioplankton (0.22–200 μm) and introducing nested PCR to amplification, we retrieved abundant pufM fragments (136 sequences in 37 OTUs) directly from upper twilight zone samples. AAPB populations in upper twilight zones covered major subgroups found in surface waters and had a slightly lower diversity, higher dominance, and lower GC and GC3 contents in pufM genes than those in surface AAPB populations. These diversity data combined with previous BChl.a data in upper twilight zones support the hypothesis that AAPB may be present below euphotic zones based on the speculation that AAPB can utilize the dim light in twilight zones as a supplement to energy supply in their heterotrophic lives.


Indian Ocean Clone Library Particulate Organic Carbon Open Ocean Euphotic Zone 



We thank Ning Hong for the help in sampling. This work was supported by the NSFC project (40632013), the MOST projects (2007CB815900 and 2006BAC11B04), the AOMRRD’s 11th 5-year programme (DYXM-115-02-4-3), the MOE project (704029) and the SOA project (200805068). The experiments comply with current Chinese laws.


  1. Achenbach LA, Carey J, Madigan MT (2001) Photosynthetic and phylogenetic primers for detection of anoxygenic phototrophs in natural environments. Appl Environ Microbiol 67:2922–2926CrossRefGoogle Scholar
  2. Allgaier M, Uphoff H, Felske A, Wagner-Dobler I (2003) Aerobic anoxygenic photosynthesis in Roseobacter clade bacteria from diverse marine habitats. Appl Environ Microbiol 69:5051–5059CrossRefGoogle Scholar
  3. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2006) New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl Environ Microbiol 72:5734–5741CrossRefGoogle Scholar
  4. Beatty JT (2002) On the natural selection and evolution of the aerobic phototrophic bacteria. Photosyn Res 73:109–114CrossRefGoogle Scholar
  5. Beatty JT, Overmann J, Lince MT, Manske AK, Lang AS, Blankenship RE, Van Dover CL, Martinson TA, Plumley FG (2005) An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent. Proc Natl Acad Sci USA 102:9306–9310CrossRefGoogle Scholar
  6. Beja O, Suzuki MT, Heidelberg JF, Nelson WC, Preston CM, Hamada T, Eisen JA, Fraser CM, DeLong EF (2002) Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature 415:630–633CrossRefGoogle Scholar
  7. Biebl H, Allgaier M, Lunsdorf H, Pukall R, Tindall BJ, Wagner-Dobler I (2005a) Roseovarius mucosus sp nov., a member of the Roseobacter clade with trace amounts of bacteriochlorophyll a. Int J Syst Evol Microbiol 55:2377–2383CrossRefGoogle Scholar
  8. Biebl H, Allgaier M, Tindall BJ, Koblizek M, Lunsdorf H, Pukall R, Wagner-Dobler I (2005b) Dinoroseobacter shibae gen. nov., sp nov., a new aerobic phototrophic bacterium isolated from dinoflagellates. Int J Syst Evol Microbiol 55:1089–1096CrossRefGoogle Scholar
  9. Biebl H, Tindall BJ, Pukall R, Lunsdorf H, Allgaier M, Wagner-Dobler I (2006) Hoeflea phototrophica sp nov., a novel marine aerobic alphaproteobacterium that forms bacteriochlorophyll a. Int J Syst Evol Microbiol 56:821–826CrossRefGoogle Scholar
  10. Biebl H, Pukall R, Lunsdorf H, Schulz S, Allgaier M, Tindall BJ, Wagner-Dobler I (2007) Description of Labrenzia alexandrii gen. nov., sp nov., a novel alphaproteobacterium containing bacterlochlorophyll a, and a proposal for reclassification of Stappia aggregata as Labrenzia aggregata comb. nov., of Stappia marina as Labrenzia marina comb. nov and of Stappia alba as Labrenzia alba comb. nov., and emended descriptions of the genera Pannonibacter, Stappia and Roseibium, and of the species Roseibium denhamense and Roseibium hamelinense. Int J Syst Evol Microbiol 57:1095–1107CrossRefGoogle Scholar
  11. Cottrell MT, Mannino A, Kirchman DL (2006) Aerobic anoxygenic phototrophic bacteria in the Mid-Atlantic Bight and the North Pacific Gyre. Appl Environ Microbiol 72:557–564CrossRefGoogle Scholar
  12. DeLong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard NU, Martinez A, Sullivan MB, Edwards R, Brito BR, Chisholm SW, Karl DM (2006) Community genomics among stratified microbial assemblages in the ocean’s interior. Science 311:496–503CrossRefGoogle Scholar
  13. Des Marais DJ (2000) Evolution—When did photosynthesis emerge on earth? Science 289:1703–1705Google Scholar
  14. Du HL, Jiao NZ, Hu YH, Zeng YH (2006) Real-time PCR for quantification of aerobic anoxygenic phototrophic bacteria based on pufM gene in marine environment. J Exp Mar Biol Ecol 329:113–121CrossRefGoogle Scholar
  15. Eiler A (2006) Evidence for the ubiquity of mixotrophic bacteria in the upper ocean: implications and consequences. Appl Environ Microbiol 72:7431–7437CrossRefGoogle Scholar
  16. Foerstner KU, von Mering C, Hooper SD, Bork P (2005) Environments shape the nucleotide composition of genomes. EMBO Rep 6:1208–1213CrossRefGoogle Scholar
  17. Fuchs B, Spring S, Teeling H, Quast C, Wulf J, Schattenhofer M, Yan S, Ferriera S, Johnson J, Glöckner F, Amann R (2007) Characterization of the first marine gammaproteobacterium capable of aerobic anoxygenic photosynthesis. Proc Natl Acad Sci USA 104:2891–2896CrossRefGoogle Scholar
  18. Fuhrman J, Comeau D, Hagstrom A, Chan A (1988) Extraction from natural planktonic microorganisms of DNA suitable for molecular biological studies. Appl Environ Microbiol 54:1426–1429PubMedPubMedCentralGoogle Scholar
  19. 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 47:345–357CrossRefGoogle Scholar
  20. Hu YH, Du HL, Jiao NZ, Zeng YH (2006) Abundant presence of the gamma-like Proteobacterial pufM gene in oxic seawater. FEMS Microbiol Lett 263:200–206CrossRefGoogle Scholar
  21. Jeffrey S, Mantoura R, Wright S (1997) Phytoplankton pigments in Oceanography. UNESCO Publishing, ParisGoogle Scholar
  22. Jiao NZ, Feng FY, Wei B (2006) Proteorhodopsin—a new path for biological utilization of light energy in the sea. Chin Sci Bull 51:889–896CrossRefGoogle Scholar
  23. Jiao NZ, Zhang Y, Zeng YH, Hong N, Liu RL, Chen F, Wang PX (2007) Distinct distribution pattern of abundance and diversity of aerobic anoxygenic phototrophic bacteria in the global ocean. Environ Microbiol 9:3091–3099CrossRefGoogle Scholar
  24. Kara AB, Rochford PA, Hurlburt HE (2003) Mixed layer depth variability over the global ocean. J Geophys Res Oceans, 108. doi:
  25. Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–510CrossRefGoogle Scholar
  26. Koblizek M, Beja O, Bidigare RR, Christensen S, Benitez-Nelson B, Vetriani C, Kolber MK, Falkowski PG, Kolber ZS (2003) Isolation and characterization of Erythrobacter sp strains from the upper ocean. Arch Microbiol 180:327–338CrossRefGoogle Scholar
  27. Koblizek M, Masin M, Ras J, Poulton AJ, Prasil O (2007) Rapid growth rates of aerobic anoxygenic phototrophs in the ocean. Environ Microbiol 9:2401–2406CrossRefGoogle Scholar
  28. Kolber ZS, Van Dover CL, Niederman RA, Falkowski PG (2000) Bacterial photosynthesis in surface waters of the open ocean. Nature 407:177–179CrossRefGoogle Scholar
  29. Kolber ZS, Plumley FG, Lang AS, Beatty JT, Blankenship RE, VanDover CL, Vetriani C, Koblizek M, Rathgeber C, Falkowski PG (2001) Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292:2492–2495CrossRefGoogle Scholar
  30. Lami R, Cottrell MT, Ras J, Ulloa O, Obernosterer I, Claustre H, Kirchman DL, Lebaron P (2007) High abundances of aerobic anoxygenic photosynthetic bacteria in the South Pacific Ocean. Appl Environ Microbiol 73:4198–4205CrossRefGoogle Scholar
  31. Martín-Cuadrado A, López-García P, Alba J, Moreira D, Monticelli L, Strittmatter A, Gottschalk G, Rodríguez-Valera F (2007) Metagenomics of the deep Mediterranean, a warm bathypelagic habitat. PloS One 2:e914CrossRefGoogle Scholar
  32. Masin M, Zdun A, Ston-Egiert J, Nausch M, Labrenz M, Moulisova V, Koblizek M (2006) Seasonal changes and diversity of aerobic anoxygenic phototrophs in the Baltic Sea. Aquat Microb Ecol 45:247–254CrossRefGoogle Scholar
  33. Masín M, Nedoma J, Pechar L, Koblízek M (2008) Distribution of aerobic anoxygenic phototrophs in temperate freshwater systems. Environ Microbiol 10:1988–1996CrossRefGoogle Scholar
  34. Musto H, Naya H, Zavala A, Romero H, Alvarez-Valin F, Bernardi G (2006) Genomic GC level, optimal growth temperature, and genome size in prokaryotes. Biochem Biophys Res Commun 347:1–3CrossRefGoogle Scholar
  35. Odum EP (1971) Principles and concepts pertaining to organization at the community level. In: Odum EP (ed) Fundamentals of ecology. Saunders College Publishing, Philadelphia, pp 140–161Google Scholar
  36. Overmann J, Garcia-Pichel F (2002) The phototrophic way of life. In: Dworkin M (ed) The prokaryotes: an evolving electronic resource for the microbiological community [online]. Springer, New YorkGoogle Scholar
  37. Oz A, Sabehi G, Koblizek M, Massana R, Beja O (2005) Roseobacter-like bacteria in Red and Mediterranean Sea aerobic anoxygenic photosynthetic populations. Appl Environ Microbiol 71:344–353CrossRefGoogle Scholar
  38. Partensky F, Hess WR, Vaulot D (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63:106–127PubMedPubMedCentralGoogle Scholar
  39. Rathgeber C, Beatty JT, Yurkov V (2004) Aerobic phototrophic bacteria: new evidence for the diversity, ecological importance and applied potential of this previously overlooked group. Photosynth Res 81:113–128CrossRefGoogle Scholar
  40. Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu DY, 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 YH, Falcon 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 5:398–431CrossRefGoogle Scholar
  41. Salka I, Moulisová V, Koblížek M, Jost G, Jürgens K, Labrenz M (2008) Abundance, depth distribution, and composition of aerobic bacteriochlorophyll a-producing bacteria in four basins of the central Baltic Sea. Appl Environ Microbiol. doi: CrossRefGoogle Scholar
  42. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506CrossRefGoogle Scholar
  43. Schloss PD, Larget BR, Handelsman J (2004) Integration of microbial ecology and statistics: a test to compare gene libraries. Appl Environ Microbiol 70:5485–5492CrossRefGoogle Scholar
  44. Schwalbach MS, Fuhrman JA (2005) Wide-ranging abundances of aerobic anoxygenic phototrophic bacteria in the world ocean revealed by epifluorescence microscopy and quantitative PCR. Limnol Oceanogr 50:620–628CrossRefGoogle Scholar
  45. 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 14:140–145CrossRefGoogle Scholar
  46. Shiba T, Simidu U (1982) Erythrobacter longus gen. nov., sp. nov., an aerobic bacterium which contains bacteriochlorophyll a. Int J Syst Bacteriol 32:211–217CrossRefGoogle Scholar
  47. Shiba T, Simidu U, Taga N (1979) Distribution of aerobic bacteria which contain bacteriochlorophyll a. Appl Environ Microbiol 38:43–45PubMedPubMedCentralGoogle Scholar
  48. Sieracki ME, Gilg IC, Thier EC, Poulton NJ, Goericke R (2006) Distribution of planktonic aerobic anoxygenic photoheterotrophic bacteria in the northwest Atlantic. Limnol Oceanogr 51:38–46CrossRefGoogle Scholar
  49. Suzuki T, Muroga Y, Takahama M, Nishimura Y (2000) Roseibium denhamense gen. nov., sp, nov and Roseibium hamelinense sp nov., aerobic bacteriochlorophyll-containing bacteria isolated from the east and west coasts of Australia. Int J Syst Evol Microbiol 50:2151–2156CrossRefGoogle Scholar
  50. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefGoogle Scholar
  51. Trujillo A, Thurman H (2004) Essentials of oceanography. Prentice Hall, ChicagoGoogle Scholar
  52. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu DY, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74CrossRefGoogle Scholar
  53. Waidner LA, Kirchman DL (2005) Aerobic anoxygenic photosynthesis genes and operons in uncultured bacteria in the Delaware River. Environ Microbiol 7:1896–1908CrossRefGoogle Scholar
  54. Waidner LA, Kirchman DL (2007) Aerobic anoxygenic phototrophic bacteria attached to particles in turbid waters of the Delaware and Chesapeake estuaries. Appl Environ Microbiol 73:3936–3944CrossRefGoogle Scholar
  55. Waidner LA, Kirchman DL (2008) Diversity and distribution of ecotypes of the aerobic anoxygenic phototrophy gene, pufM, in the Delaware estuary. Appl Environ Microbiol 74:4012–4021CrossRefGoogle Scholar
  56. Yurkov VV, Beatty JT (1998) Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62:695–724PubMedPubMedCentralGoogle Scholar
  57. Yurkov VV, Krieger S, Stackebrandt E, Beatty JT (1999) Citromicrobium bathyomarinum, a novel aerobic bacterium isolated from deep-sea hydrothermal vent plume waters that contains photosynthetic pigment–protein complexes. J Bacteriol 181:4517–4525PubMedPubMedCentralGoogle Scholar
  58. Yutin N, Suzuki MT, Beja O (2005) Novel primers reveal wider diversity among marine aerobic anoxygenic phototrophs. Appl Environ Microbiol 71:8958–8962CrossRefGoogle Scholar
  59. Yutin N, Suzuki MT, Teeling H, Weber M, Venter JC, Rusch DB, Beja O (2007) Assessing diversity and biogeography of aerobic anoxygenic phototrophic bacteria in surface waters of the Atlantic and Pacific Oceans using the Global Ocean Sampling expedition metagenomes. Environ Microbiol 9:1464–1475CrossRefGoogle Scholar
  60. Zeng YH, Jiao NZ (2007) Source environment feature related phylogenetic distribution pattern of anoxygenic photosynthetic bacteria as revealed by pufM analysis. J Microbiol 45:205–212PubMedGoogle Scholar
  61. Zeng YH, Jiao NZ, Cai HY, Chen XH, Wei CL (2004) Phylogenetic diversity of ribulose-1, 5-bisphosphate carboxylase/oxygenase large subunit genes of bacterioplankton in the East China Sea. Acta Oceanol Sin 23:673–685Google Scholar
  62. Zeng YH, Chen XH, Jiao NZ (2007) Genetic diversity assessment of anoxygenic photosynthetic bacteria by distance-based grouping analysis of pufM sequences. Lett Appl Microbiol 45:639–645CrossRefGoogle Scholar
  63. Zhang Y, Jiao N (2007) Dynamics of aerobic anoxygenic phototrophic bacteria in the East China Sea. FEMS Microbiol Ecol 61:459–469CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.State Key Laboratory of Marine Environmental ScienceXiamen UniversityXiamenPeople’s Republic of China

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