Advertisement

Acta Oceanologica Sinica

, Volume 35, Issue 6, pp 68–77 | Cite as

Diversity of the aerobic anoxygenic phototrophy gene pufM in Arctic and Antarctic coastal seawaters

  • Yinxin ZengEmail author
  • Peiyan Dong
  • Zongyun Qiao
  • Tianling Zheng
Article

Abstract

Aerobic anoxygenic phototrophic (AAP) bacteria serve important functions in marine carbon and energy cycling because of their capability to utilize dissolved organic substrates and harvest light energy. AAP bacteria are widely distributed in marine environments, and their diversity has been examined in marine habitats. However, information about AAP bacteria at high latitudes remains insufficient to date. Therefore, this study determined the summer AAP bacterial diversity in Arctic Kongsfjorden and in the Antarctic coastal seawater of King George Island on the basis of pufM, a gene that encodes a pigment-binding protein subunit of the reaction center complex. Four pufM clone libraries were constructed, and 674 positive clones were obtained from four investigated stations (two in Kongsfjorden and two in the Antarctic Maxwell Bay). Arctic clones were clustered within the Alphaproteobacteria, whereas Antarctic clones were classified into the Alphaproteobacteria and Betaproteobacteria classes. Rhodobacteraceae-like pufM genes dominated in all samples. In addition, sequences closely related to pufM encoded on a plasmid in Sulfitobacter guttiformis were predominant in both Arctic and Antarctic samples. This result indicates the transpolar or even global distribution of pufM genes in marine environments. Meanwhile, differences between the Arctic and Antarctic sequences may prove polar endemism. These results indicate the important role of Rhodobacteraceae as AAP bacteria in bipolar coastal waters.

Keywords

diversity aerobic anoxygenic phototrophic bacteria pufM Arctic Antarctic 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Achenbach L A, Carey J, Madigan M T. 2001. Photosynthetic and phylogenetic primers for detection of anoxygenic phototrophs in natural environments. Applied and Environmental Microbiology, 67(7): 2922–2926CrossRefGoogle Scholar
  2. Bano N, Hollibaugh J T. 2000. Diversity and distribution of DNA sequences with affinity to ammonia-oxidizing bacteria of the β-subdivision of the class Proteobacteria in the Arctic Ocean. Applied and Environmental Microbiology, 66(5): 1960–1969CrossRefGoogle Scholar
  3. Beatty J T. 2002. On the natural selection and evolution of the aerobic phototrophic bacteria. Photosynthesis Research, 73(1–3): 109–114CrossRefGoogle Scholar
  4. Béjà O, Suzuki M T, Heidelberg J F, et al. 2002. Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature, 415(6872): 630–633CrossRefGoogle Scholar
  5. Boeuf D, Cottrell M T, Kirchman D L, et al. 2013. Summer community structure of aerobic anoxygenic phototrophic bacteria in the western Arctic Ocean. FEMS Microbiology Ecology, 85(3): 417–432CrossRefGoogle Scholar
  6. Bosshard P P, Santini Y, Grüter D, et al. 2000. Bacterial diversity and community composition in the chemocline of the meromictic alpine Lake Cadagno as revealed by 16S rDNA analysis. FEMS Microbiology Ecology, 31(2): 173–182CrossRefGoogle Scholar
  7. Cottier F, Tverberg V, Inall M, et al. 2005. Water mass modification in an Arctic fjord through cross-shelf exchange: the seasonal hydrography of Kongsfjorden, Svalbard. Journal of Geophysical Research, 110(C12): C12005CrossRefGoogle Scholar
  8. Cottrell M T, Kirchman D L. 2009. Photoheterotrophic microbes in the Arctic Ocean in summer and winter. Applied and Environmental Microbiology, 75(15): 4958–4966CrossRefGoogle Scholar
  9. Cottrell M T, Mannino A, Kirchman D L. 2006. Aerobic anoxygenic phototrophic bacteria in the Mid-Atlantic Bight and the North Pacific Gyre. Applied and Environmental Microbiology, 72(1): 557–564CrossRefGoogle Scholar
  10. Cottrell M T, Ras J, Kirchman D L. 2010. Bacteriochlorophyll and community structure of aerobic anoxygenic phototrophic bacteria in a particle-rich estuary. The ISME Journal, 4(7): 945–954CrossRefGoogle Scholar
  11. De Corte D, Sintes E, Yokokawa T, et al. 2013. Comparison between MICRO-CARD-FISH and 16S rRNA gene clone libraries to assess the active versus total bacterial community in the coastal Arctic. Environmental Microbiology Reports, 5(2): 272–281CrossRefGoogle Scholar
  12. Ferrera I, Borrego C M, Salazar G, et al. 2014. Marked seasonality of aerobic anoxygenic phototrophic bacteria in the coastal NW Mediterranean Sea as revealed by cell abundance, pigment concentration and pyrosequencing of pufM gene. Environmental Microbiology, 16(9): 2953–2965CrossRefGoogle Scholar
  13. Ghiglione J F, Galand P E, Pommier T, et al. 2012. Pole-to-pole biogeography of surface and deep marine bacterial communities. Proceedings of the National Academy of Sciences of the United States America, 109(43): 17633–17638CrossRefGoogle Scholar
  14. Hojerová E, Mašín M, Brunet C, et al. 2011. Distribution and growth of aerobic anoxygenic phototrophs in the Mediterranean Sea. Environmental Microbiology, 13(10): 2717–2725CrossRefGoogle Scholar
  15. Hollibaugh J T, Bano N, Ducklow H W. 2002. Widespread distribution in polar oceans of a 16S rRNA gene sequence with affinity to Nitrosospira-like ammonia-oxidizing bacteria. Applied and Environmental Microbiology, 68(3): 1478–1484CrossRefGoogle Scholar
  16. Huber T, Faulkner G, Hugenholtz P. 2004. Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics, 20(14): 2317–2319CrossRefGoogle Scholar
  17. Jeanthon C, Boeuf D, Dahan O, et al. 2011. Diversity of cultivated and metabolically active aerobic anoxygenic phototrophic bacteria along an oligotrophic gradient in the Mediterranean Sea. Biogeosciences, 8(7): 1955–1970CrossRefGoogle Scholar
  18. Jiao Nianzhi, Zhang Yao, Zeng Yonghui, et al. 2007. Distinct distribution pattern of abundance and diversity of aerobic anoxygenic phototrophic bacteria in the global ocean. Environmental Microbiology, 9(12): 3091–3099CrossRefGoogle Scholar
  19. Khim B K, Yoon H I. 2003. Postglacial marine environmental changes in Maxwell Bay, King George Island, West Antarctica. Polar Research, 22(2): 341–353CrossRefGoogle Scholar
  20. Kirchman D L, Stegman M R, Nikrad M P, et al. 2014. Abundance, size, and activity of aerobic anoxygenic phototrophic bacteria in coastal waters of the West Antarctic Peninsula. Aquatic Microbial Ecology, 73(1): 41–49CrossRefGoogle Scholar
  21. Koblížek M, Béjà O, Bidigare R R, et al. 2003. Isolation and characterization of Erythrobacter sp. strains from the upper ocean. Archives of Microbiology, 180(5): 327–338CrossRefGoogle Scholar
  22. Koblížek M, Moulisová V, Muronová M, et al. 2015. Horizontal transfers of two types of puf operons among phototrophic members of the Roseobacter clade. Folia Microbiologica, 60(1): 37–43CrossRefGoogle Scholar
  23. Koh E Y, Martin A R, McMinn A, et al. 2012. Recent advances and future perspectives in microbial phototrophy in Antarctic sea ice. Biology, 1(3): 542–556CrossRefGoogle Scholar
  24. Koh E Y, Phua W, Ryan K G. 2011. Aerobic anoxygenic phototrophic bacteria in Antarctic sea ice and seawater. Environmental Microbiology Reports, 3(6): 710–716CrossRefGoogle Scholar
  25. Kolber Z S, Van Dover C L, Niederman R A, et al. 2000. Bacterial photosynthesis in surface waters of the open ocean. Nature, 407(6801): 177–179CrossRefGoogle Scholar
  26. Kolber Z S, Plumley F G, Lang A S, et al. 2001. Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science, 292(5526): 2492–2495CrossRefGoogle Scholar
  27. Lami R, Cottrell M T, Ras J, et al. 2007. High abundances of aerobic anoxygenic photosynthetic bacteria in the South Pacific Ocean. Applied and Environmental Microbiology, 73(13): 4198–4205CrossRefGoogle Scholar
  28. Lehours A C, Cottrell M T, Dahan O, et al. 2010. Summer distribution and diversity of aerobic anoxygenic phototrophic bacteria in the Mediterranean Sea in relation to environmental variables. FEMS Microbiology Ecology, 74(2): 397–409CrossRefGoogle Scholar
  29. López O, García M A, Arcilla A S. 1994. Tidal and residual currents in the Bransfield Strait, Antarctica. Annales Geophysicae, 12(9): 887–902CrossRefGoogle Scholar
  30. Nedzarek A. 2008. Sources, diversity and circulation of biogenic compounds in Admiralty Bay, King George Island, Antarctica. Antarctic Science, 20(2): 135–145CrossRefGoogle Scholar
  31. Nelson Silva S, Helbling E W, Villafañe V, et al. 1995. Variability in nutrient concentrations around Elephant Island, Antarctica, during 1991–1993. Polar Research, 14(1): 69–82CrossRefGoogle Scholar
  32. Oz A, Sabehi G, Koblízek M, et al. 2005. Roseobacter-like bacteria in Red and Mediterranean Sea aerobic anoxygenic photosynthetic populations. Applied and Environmental Microbiology, 71(1): 344–353CrossRefGoogle Scholar
  33. Piquet A M T, Scheepens J F, Bolhuis H, et al. 2010. Variability of protistan and bacterial communities in two Arctic fjords (Spitsbergen). Polar Biology, 33(11): 1521–1536CrossRefGoogle Scholar
  34. Pradella S, Allgaier M, Hoch C, et al. 2004. Genome organization and localization of the pufLM genes of the photosynthesis reaction center in phylogenetically diverse marine Alphaproteobacteria. Applied and Environmental Microbiology, 70(6): 3360–3369CrossRefGoogle Scholar
  35. Ravenschlag K, Sahm K, Pernthaler J, et al. 1999. High bacterial diversity in permanently cold marine sediments. Applied and Environmental Microbiology, 65(9): 3982–3989Google Scholar
  36. Schloss P D, Handelsman J. 2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Applied and Environmental Microbiology, 71(3): 1501–1506CrossRefGoogle Scholar
  37. Schloss P D, Westcott S L, Ryabin T, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75(23): 7537–7541CrossRefGoogle Scholar
  38. Schwalbach M S, Fuhrman J A. 2005. Wide-ranging abundances of aerobic anoxygenic phototrophic bacteria in the world ocean revealed by epifluorescence microscopy and quantitative PCR. Limnology and Oceanography, 50(2): 620–628CrossRefGoogle Scholar
  39. Shiba T, Harashima K. 1986. Aerobic photosynthetic bacteria. Microbiology Science, 3(12): 376–378Google Scholar
  40. Sieracki M E, Gilg I C, Thier E C, et al. 2006. Distribution of planktonic aerobic anoxygenic photoheterotrophic bacteria in the northwest Atlantic. Limnology and Oceanography, 51(1): 38–46CrossRefGoogle Scholar
  41. Søndergaard M, Middelboe M. 1995. A cross-system analysis of labile dissolved organic carbon. Marine Ecology Progress Series, 118: 283–294CrossRefGoogle Scholar
  42. Sul W J, Oliver T A, Ducklow H W, et al. 2013. Marine bacteria exhibit a bipolar distribution. Proceedings of the National Academy of Sciences of the United States America, 110(6): 2342–2347CrossRefGoogle Scholar
  43. Svendsen H, Beszczynska-Møller A, Hagen J O, et al. 2002. The physical environment of Kongsfjorden-Krossfjorden, an Arctic fjord system in Svalbard. Polar Research, 21(1): 133–166CrossRefGoogle Scholar
  44. Tamura K, Peterson D, Peterson N, et al. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10): 2731–2739CrossRefGoogle Scholar
  45. Tank M, Blümel M, Imhoff J F. 2011. Communities of purple sulfur bacteria in a Baltic Sea coastal lagoon analyzed by puf LM gene libraries and the impact of temperature and NaCl concentration in experimental enrichment cultures. FEMS Microbiology Ecology, 78(3): 428–438CrossRefGoogle Scholar
  46. Thiel V, Tank M, Neulinger S C, et al. 2010. Unique communities of anoxygenic phototrophic bacteria in saline lakes of Salar de Atacama (Chile): evidence for a new phylogenetic lineage of phototrophic Gammaproteobacteria from pufLM gene analyses. FEMS Microbiology Ecology, 74(3): 510–522CrossRefGoogle Scholar
  47. Waidner L A, Kirchman D L. 2008. Diversity and distribution of ecotypes of the aerobic anoxygenic phototrophy gene pufM in the Delaware estuary. Applied and Environmental Microbiology, 74(13): 4012–4021CrossRefGoogle Scholar
  48. Yurkov V, Csotonyi J T. 2009. New light on aerobic anoxygenic phototrophs. In: Hunter C N, Daldal F, Thurnauer M C, et al., eds. The Purple Phototrophic Bacteria. Netherlands: Springer, 31–55CrossRefGoogle Scholar
  49. Yutin N, Suzuki M T, Béjà O. 2005. Novel primers reveal wider diversity among marine aerobic anoxygenic phototrophs. Applied and Environmental Microbiology, 71(12): 8958–8962CrossRefGoogle Scholar
  50. Yutin N, Suzuki M T, Teeling H, et al. 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. Environmental Microbiology, 9(6): 1464–1475CrossRefGoogle Scholar
  51. Zeng Yinxin, Yu Yong, Qiao Zongyun, et al. 2014. Diversity of bacterioplankton in coastal seawaters of Fildes Peninsula, King George Island, Antarctica. Archives of Microbiology, 196(2): 137–147CrossRefGoogle Scholar
  52. Zeng Yinxin, Zhang Fang, He Jianfeng, et al. 2013. Bacterioplankton community structure in the Arctic waters as revealed by pyrosequencing of 16S rRNA genes. Antonie van Leeuwenhoek, 103(6): 1309–1319CrossRefGoogle Scholar
  53. Zeng Yinxin, Zheng Tianling, Li Huirong. 2009. Community composition of the marine bacterioplankton in Kongsfjorden (Spitsbergen) as revealed by 16S rRNA gene analysis. Polar Biology, 32(10): 1447–1460CrossRefGoogle Scholar
  54. Zheng Qiang, Liu Yanting, Steindler L, et al. 2015. Pyrosequencing analysis of aerobic anoxygenic phototrophic bacterial community structure in the oligotrophic western Pacific Ocean. FEMS Microbiology Letters, 362(8): fnv034, doi: 10.1093/femsle/fnv034CrossRefGoogle Scholar

Copyright information

© The Chinese Society of Oceanography and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Yinxin Zeng
    • 1
    • 2
    Email author
  • Peiyan Dong
    • 3
  • Zongyun Qiao
    • 1
    • 2
  • Tianling Zheng
    • 3
  1. 1.Key Laboratory for Polar Science of State Oceanic AdministrationPolar Research Institute of ChinaShanghaiChina
  2. 2.College of Biological EngineeringJimei UniversityXiamenChina
  3. 3.State Key Laboratory of Marine Environmental Science, School of Life SciencesXiamen UniversityXiamenChina

Personalised recommendations