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Abundance and diversity of archaeal accA gene in hot springs in Yunnan Province, China

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Abstract

It has been suggested that archaea carrying the accA gene, encoding the alpha subunit of the acetyl CoA carboxylase, autotrophically fix CO2 using the 3-hydroxypropionate/4-hydroxybutyrate pathway in low-temperature environments (e.g., soils, oceans). However, little new information has come to light regarding the occurrence of archaeal accA genes in high-temperature ecosystems. In this study, we investigated the abundance and diversity of archaeal accA gene in hot springs in Yunnan Province, China, using DNA- and RNA-based phylogenetic analyses and quantitative polymerase chain reaction. The results showed that archaeal accA genes were present and expressed in the investigated Yunnan hot springs with a wide range of temperatures (66–96 °C) and pH (4.3–9.0). The majority of the amplified archaeal accA gene sequences were affiliated with the ThAOA/HWCG III [thermophilic ammonia-oxidizing archaea (AOA)/hot water crenarchaeotic group III]. The archaeal accA gene abundance was very close to that of AOA amoA gene, encoding the alpha subunit of ammonia monooxygenase. These data suggest that AOA in terrestrial hot springs might acquire energy from ammonia oxidation coupled with CO2 fixation using the 3-hydroxypropionate/4-hydroxybutyrate pathway.

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References

  • Auguet JC, Borrego CM, Bañeras L, Casamayor EO (2008) Fingerprinting the genetic diversity of the biotin carboxylase gene (accC) in aquatic ecosystems as a potential marker for studies of carbon dioxide assimilation in the dark. Environ Microbiol 10:2527–2536

    Article  PubMed  CAS  Google Scholar 

  • Berg IA (2011) Ecological aspects of the distribution of different autotrophic CO2 fixation pathways. Appl Environ Microbiol 77:1925–1936

    Article  PubMed  CAS  Google Scholar 

  • Berg IA, Kockelkorn D, Buckel W, Fuchs G (2007) A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318:1782–1786

    Article  PubMed  CAS  Google Scholar 

  • Berg IA, Kockelkorn D, Ramos-Vera WH, Say RF, Zarzycki J, Hügler M, Alber BE, Fuchs G (2010a) Autotrophic carbon fixation in archaea. Nat Rev Microbiol 8:447–460

    Article  PubMed  CAS  Google Scholar 

  • Berg IA, Ramos-Vera WH, Petri A, Huber H, Fuchs G (2010b) Study of the distribution of autotrophic CO2 fixation cycles in Crenarchaeota. Microbiology 156:256–269

    Article  PubMed  CAS  Google Scholar 

  • Brownsey RW, Zhande R, Boone AN (1997) Isoforms of acetyl-CoA carboxylase: structures, regulatory properties and metabolic functions. Biochem Soc Trans 25:1232–1238

    PubMed  CAS  Google Scholar 

  • Chao A (2010) SPADE: species prediction and diversity estimation. URL http://chao.stat.nthu.edu.tw/softwareCE.html

  • Dawson S, DeLong E, Pace NR (2006) Phylogenetic and ecological perspectives on uncultured crenarchaeota and korarchaeota. In: Dworkin M (ed) The Prokaryotes. Springer-Verlag, Berlin Release 3.7

    Google Scholar 

  • de la Torre JR, Walker CB, Ingalls AE, Konneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10:810–818

    Article  PubMed  Google Scholar 

  • Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia oxidizing archaea. FEMS Microbiol Rev 33:855–869

    Article  PubMed  CAS  Google Scholar 

  • Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102:14683–14688

    Article  PubMed  CAS  Google Scholar 

  • Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, James P, Schloter M, Griffiths RI, Prosser JI, Nicol GW (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci USA 108:21206–21211

    Article  PubMed  CAS  Google Scholar 

  • Hallam SJ, Mincer TJ, Schleper C, Preston CM, Roberts K, Richardson PM, DeLong EF (2006) Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol 4:e95

    Article  PubMed  Google Scholar 

  • Hatzenpichler R (2012) Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microbiol 78:7501–7510

    Article  PubMed  CAS  Google Scholar 

  • Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M (2008) A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci USA 105:2134–2139

    Article  PubMed  CAS  Google Scholar 

  • Hu A, Jiao N, Zhang CL (2011a) Community structure and function of planktonic Crenarchaeota: changes with depth in the South China Sea. Microb Ecol 62:549–563

    Article  PubMed  CAS  Google Scholar 

  • Hu A, Jiao N, Zhang R, Yang Z (2011b) Niche partitioning of marine group I Crenarchaeota in the euphotic and upper mesopelagic zones of the East China Sea. Appl Environ Microbio 77:7469–7478

    Article  CAS  Google Scholar 

  • Huber H, Gallenberger M, Jahn U, Eylert E, Berg IA, Kockelkorn D, Eisenreich W, Fuchs G (2008) A dicarboxylate/4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic Archaeum Ignicoccus hospitalis. Proc Natl Acad Sci USA 105:7851–7856

    Article  PubMed  CAS  Google Scholar 

  • Jiang H, Dong H, Deng S, Yu B, Huang Q, Wu Q (2009) Response of archaeal community structure to environmental changes in lakes on the Tibetan Plateau, northwestern China. Geomicrobiol J 26:289–297

    Article  CAS  Google Scholar 

  • Jiang H, Huang Q, Dong H, Wang P, Wang F, Li W, Zhang CL (2010) RNA-based investigation of ammonia-oxidizing archaea in hot springs of Yunnan Province, China. Appl Environ Microbiol 76:2541–4538

    Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA Sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley Sons, New York, pp 115–175

    Google Scholar 

  • Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW (2011) Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc Natl Acad Sci USA 108:15892–15897

    Article  PubMed  CAS  Google Scholar 

  • Moss J, Lane MD (1971) Biotin-dependent enzymes. Adv Enzymol Relat Areas Mol Biol 35:321–442

    PubMed  CAS  Google Scholar 

  • Nadkarni M, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad range (universal) probe and primer set. Microbiology 148:257–266

    PubMed  CAS  Google Scholar 

  • Nunoura T, Hirayama H, Takami H, Oida H, Nishi S, Shimamura S, Suzuki Y, Inagaki F, Takai K, Nealson KH, Horikoshi K (2005) Genetic and functional properties of uncultivated thermophilic crenarchaeotes from a subsurface gold mine as revealed by analysis of genome fragments. Environ Microbiol 7:1967–1984

    Article  PubMed  CAS  Google Scholar 

  • Pratscher J, Dumont MG, Conrad R (2011) Ammonia oxidation coupled to CO2 fixation by archaea and bacteria in an agricultural soil. Proc Natl Acad Sci USA 108:4170–4175

    Article  PubMed  CAS  Google Scholar 

  • Reigstad LJ, Richter A, Daims H, Urich T, Schwark L, Schleper C (2008) Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol 64:167–174

    Article  PubMed  CAS  Google Scholar 

  • Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506

    Article  PubMed  CAS  Google Scholar 

  • Song Z, Chen J, Jiang HC, Zhou EM, Tang SK, Zhi XY, Zhang L, Zhang CL, Li W (2010) Diversity of Crenarchaeota in terrestrial hot springs in Tengchong, China. Extremophiles 14:287–296

    Article  PubMed  Google Scholar 

  • Song Z, Wang F, Zhi X, Chen J, Zhou E, Liang F, Xiao X, Tang S, Jiang H, Zhang CL, Dong H, Li W (2013) Bacterial and archaeal diversities in Yunnan and Tibetan hot springs, China. Environ Microbiol 15:1160–1175

    Article  PubMed  CAS  Google Scholar 

  • Stahl DA, de la Torre JR (2012) Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol 66:83–101

    Article  PubMed  CAS  Google Scholar 

  • Takai K, Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066–5072

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci USA 108:8420–8425

    Article  PubMed  CAS  Google Scholar 

  • Yakimov MM, Conoa VL, Denaroa R (2009) A first insight into the occurrence and expression of functional amoA and accA genes of autotrophic and ammonia-oxidizing bathypelagic Crenarchaeota of Tyrrhenian Sea. Deep Sea Res II 56:748–754

    Article  CAS  Google Scholar 

  • Yakimov MM, Cono VL, Smedile F, DeLuca TH, Juárez S, Ciordia S, Fernández M, Albar JP, Ferrer M, Golyshin PN, Giuliano L (2011) Contribution of crenarchaeal autotrophic ammonia oxidizers to the dark primary production in Tyrrhenian deep waters (Central Mediterranean Sea). ISME J 5:9459–9461

    Article  Google Scholar 

  • Zhang CL, Ye Q, Huang Z, Li W, Chen J, Song Z, Zhao W, Bagwell C, Inskeep WP, Ross C, Gao L, Wiegel J, Romanek CS, Shock EL, Hedlund BP (2008) Global occurrence of archaeal amoA genes in terrestrial hot springs. Appl Environ Microbiol 74:6417–6426

    Article  PubMed  CAS  Google Scholar 

  • Zhang LM, Offre PR, He JZ, Verhamme DT, Nicol GW, Prosser JI (2010) Autotrophic ammonia oxidation by soil thaumarchaea. Proc Natl Acad Sci USA 107:17240–17245

    Article  PubMed  CAS  Google Scholar 

  • Zhao W, Song Z, Jiang H, Li W, Mou X, Christopher SR, Juergen W, Dong H, Zhang CL (2011) Ammonia-oxidizing Archaea in Kamchatka Hot Springs. Geomicrobiol J 28:149–159

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Basic Research Program of China (No. 2010CB833801 and 2012CB822004), the National Natural Science Foundation of China (Nos. 31070007, 40972211, 41030211, 41002123, and 41120124003), the Key Project of International Cooperation of China Ministry of Science and Technology (MOST) (No. 2013DFA31980), Key Project of Yunnan Provincial Natural Science Foundation (2013FA004), Program for New Century Excellent Talents in University, MOE (NCET-12-0954), and the Fundamental Research Funds for the China Central Universities, China University of Geosciences (Wuhan). W-J Li was also supported by ‘Hundred Talents Program’ of the Chinese Academy of Sciences. The authors also thank Chaolei Jiang, Jianxin Fang, Jinchuan Yin, Shaochuan Gong, Jiafu Sheng, and Mr. Ma and the entire staff from Yunnan Tengchong Volcano and Spa Tourist Attraction Development Corporation for sampling support, and Drs JI Prosser and Laura Lehtovirta (Institute of Biological and Environmental Sciences, University of Aberdeen) for providing accA gene of Nitrosotalea devanaterra. The authors are grateful to three anonymous reviewers whose constructive comments significantly improved the quality of the manuscript.

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Correspondence to Hong-Chen Jiang or Wen-Jun Li.

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Communicated by F. Robb.

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Song, ZQ., Wang, L., Wang, FP. et al. Abundance and diversity of archaeal accA gene in hot springs in Yunnan Province, China. Extremophiles 17, 871–879 (2013). https://doi.org/10.1007/s00792-013-0570-4

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