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Extremophiles

, Volume 23, Issue 6, pp 747–757 | Cite as

Comparative evaluation of three archaeal primer pairs for exploring archaeal communities in deep-sea sediments and permafrost soils

  • Shiping WeiEmail author
  • Hongpeng Cui
  • Yuchen Zhang
  • Xin Su
  • Hailiang Dong
  • Fang Chen
  • Youhai Zhu
Original Paper

Abstract

16S rRNA gene profiling is a powerful method for characterizing microbial communities; however, no universal primer pair can target all bacteria and archaea, resulting in different primer pairs which may impact the diversity profile obtained. Here, we evaluated three pairs of high-throughput sequencing primers for characterizing archaeal communities from deep-sea sediments and permafrost soils. The results show that primer pair Arch519/Arch915 (V4–V5 regions) produced the highest alpha diversity estimates, followed by Arch349f/Arch806r (V3–V4 regions) and A751f/AU1204r (V5–V7 regions) in both sample types. The archaeal taxonomic compositions and the relative abundance estimates of archaeal communities are influenced by the primer pairs. Beta diversity of the archaeal community detected by the three primer pairs reveals that primer pairs Arch349f/Arch806r and Arch519f/Arch915r are biased toward detection of Halobacteriales, Methanobacteriales and MBG-E/Hydrothermarchaeota, whereas the primer pairs Arch519f/Arch915r and A751f/UA1204r are biased to detect MBG-B/Lokiarchaeota, and the primers pairs Arch349f/Arch806r and A751f/UA1204r are biased to detect Methanomicrobiales and Methanosarcinales. The data suggest that the alpha and beta diversities of archaeal communities as well as the community compositions are influenced by the primer pair choice. This finding provides researchers with valuable experimental insight for selection of appropriate archaeal primer pairs to characterize archaeal communities.

Keywords

High-throughput sequencing Archaeal primers Archaeal communities Deep-sea sediment Permafrost soil 

Notes

Acknowledgements

This research was supported by Funds of Oil and Gas Survey, China Geological Survey (GZH201400308). We thank Dr. Fei Liu at the Institute of Microbiology, Chinese Academy of Sciences for calculating and analyzing the archaeal beta diversity. We also thank James Hurley at the Virginia Polytechnic Institute and State University for making a critical reading and revision of this paper.

Supplementary material

792_2019_1128_MOESM1_ESM.docx (76 kb)
Supplementary file1 (DOCX 75 kb)

References

  1. Bahram M, Anslan S, Hildebrand F, Bork P, Tedersoo L (2018) Newly designed 16S rRNA metabarcoding primers amplify diverse and novel archaeal taxa from the environment. Environ Microbiol Rep 9999(9999) na–naGoogle Scholar
  2. Bai R, Wang JT, Deng Y, He JZ, Feng K, Zhang LM (2017) Microbial community and functional structure significantly varied among distinct types of paddy soils but responded differently along gradients of soil depth layers. Front Microbiol 8:945PubMedPubMedCentralGoogle Scholar
  3. Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Meth 55:541–555Google Scholar
  4. Bartram AK, Lynch MDJ, Stearns JC, Moreno-Hagelsieb G, Meufeld JD (2011) Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end Illumina reads. Appl Environ Microbiol 77:3846–3852PubMedPubMedCentralGoogle Scholar
  5. Bell TAS, Prithiviraj B, Wahlent BD, Fields MW, Peyton BM (2016) A lipid-accumulating alga maintains growth in outdoor, alkaliphilic raceway pond with mixed microbial communities. Frontiers in microbiology 6:1480.Google Scholar
  6. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336PubMedPubMedCentralGoogle Scholar
  7. Chakravorty S, Helb D, Burday M, Connell N, Alland D (2007) A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J Microbial Meth 69:330–339Google Scholar
  8. Claesson MJ, Wang Q, O’Sullivan O, Greene-Diniz R, Cole JR, Ross RP, O’Toole PW (2010) Comparison of two next-generation sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene regions. Nucleic Acids Res 38:e200PubMedPubMedCentralGoogle Scholar
  9. Coolen MJL, Hopmans EC, Rijpstra WIC, Muyzer G, Schouten S, Volkman JK, Damsté JSS (2004) Evolution of the methane cycle in ace lake (Antarctica) during the Holocene: response of methanogens and methanotrophs to environmental change. Org Geochem 35(1151):1167Google Scholar
  10. Cui H, Su X, Chen F, Wei S, Chen S, Wang J (2016) Vertical distribution of archaeal communities in cold seep sediments from the Jiulong methane reef area in the South China Sea. Biosci J 32:1059–1068Google Scholar
  11. De León KB, Gerlach R, Peyton BM, Fields MY (2013) Archaeal and bacterial communities in three alkaline hot springs in Heart Lake Geyser Basin. Yellowstone Natl Park 4:330Google Scholar
  12. Ding J, Zhang Y, Wang H, Jian H, Leng H, Xiao X (2017) Microbial community structure of deep-sea hydrothermal vents on the ultraslow spreading Southwest Indian Ridge. Front Microbiol 8:1012PubMedPubMedCentralGoogle Scholar
  13. Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL et al (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Natl Acad Sci USA 109:21390–21395PubMedGoogle Scholar
  14. Fischer MA, Güllert S, Neulinger SC, Streit WR, Schmitz RA (2016) Evaluation of 16S rRNA gene primer pairs for monitoring microbial community structures showed high reproducibility within and low comparability between datasets generated with multiple archaeal and bacterial primer pairs. Front Microbiol 7:1297PubMedPubMedCentralGoogle Scholar
  15. Fredriksson NJ, Hermansson M, Wilén BM (2013) The Choice of PCR primers has great impact on assessments of bacterial community diversity and dynamics in a wastewater treatment plant. PLoS One 8:e76431PubMedPubMedCentralGoogle Scholar
  16. Galand PE, Lucas S, Fagervold SK, Peru E, Pruski AM, Vétion G et al (2016) Disturbance increases microbial community diversity and production in marine sediments. Front Microbiol 7:1950PubMedPubMedCentralGoogle Scholar
  17. Gantner S, Andersson AF, Alonso-Sáez L, Bertilsson S (2011) Novel primers for 16S rRNA-based archaeal community analyses in environmental samples. J Microbiol Meth 84:12–18Google Scholar
  18. Genderjahn S, Alawi M, Mangelsdorf K, Horn F, Wagner D (2018) Desiccation- and saline-tolerant bacteria and archaea in Kalahari Pan sediments. Front Microbiol 9:2082PubMedPubMedCentralGoogle Scholar
  19. Ghyselinck J, Pfeiffer S, Heylen K, Sessitsch A, De Vos P (2013) The effect of primer choice and short read sequences on the outcome of 16S rRNA gene based diversity studies. PLoS One 8:e71360PubMedPubMedCentralGoogle Scholar
  20. Head IM, Saunders JR, Pickup RW (1998) Microbial evolution, diversity, and ecology: a decade of ribosomal RNA analysis of uncultivated microorganisms. Microb Ecol 35:1–21PubMedGoogle Scholar
  21. Herfort L, Kim JH, Coolen MJL, Abbas B, Schouten S, Herndl G, Damsté JSS (2009) Diversity of archaea and detection of crenarchaeotal amoA genes in the rivers Rhine and Têt. Aquat Microb Ecol 55:189–201Google Scholar
  22. Hugoni M, Taib N, Debroas D, Domaizon I, Dufournel IJ, Bronner G et al (2013) Structure of the rare archaeal biosphere and seasonal dynamics of active ecotypes in surface coastal waters. Proc Natl Acad Sci USA 110:6004–6009PubMedGoogle Scholar
  23. Jiao S, Xu Y, Zhang J, Lu Y (2019) Environmental filtering drives distinct continental atlases of soil archaea between dryland and wetland agricultural ecosystems. Microbiome 7:15PubMedPubMedCentralGoogle Scholar
  24. Jungbluth SP, Amend JP, Rappé (2017) Data descriptor: Metagenome sequencing and 98 microbial genomes from Juan de Fuca Ridge flank subsurface fluids. Sci Data 4:170037PubMedPubMedCentralGoogle Scholar
  25. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1PubMedGoogle Scholar
  26. Kuang JL, Huang LN, Chen LX, Hua ZS, Li SJ, Hu M, Li JT, Shu WS (2012) Contemporary environmental variation determines microbial diversity patterns in acid mine drainage. ISME J 5:1038–1050Google Scholar
  27. Kubo K, Lloyd KG, Biddle JF, Amann R, Teske A, Knittel K (2012) Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diversity and widespread in marine sediments. ISME J 6:1949–1965PubMedPubMedCentralGoogle Scholar
  28. Lauer A, Sørensen KB, Teske A (2016) Phylogenetic characterization of marine benthic archaea in organic-poor sediments of the eastern equatorial pacific ocean (ODP site 1225). Microorganisms 4:32PubMedCentralGoogle Scholar
  29. Lazarevic V, Whiteson K, Huse S, Hernandez D, Farinelli L, Osteras M, Schrenzel J, Francois P (2009) Metagenomic study of the oral microbiota by Illumina high-throughput sequencing. J Microbiol Meth 79:266–271Google Scholar
  30. Liebner S, Ganzert L, Kiss A, Yang S, Wagner D, Svenning MM (2015) Shifts in methanogenic community composition and methane fluxes along the degradation of discontinuous permafrost. Front Microbiol 6:356PubMedPubMedCentralGoogle Scholar
  31. Liu Z, Lozupone C, Hamady M, Bushman FD, Knight R (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35:e120PubMedPubMedCentralGoogle Scholar
  32. Liu X, Fan H, Ding X, Hong Z, Nei Y, Liu Z, Li G, Guo H (2014a) Analysis of the gut microbiota by high-throughput sequencing of the V5–V6 regions of the 16S rRNA gene in Donkey. Curr Microbiol 68:657–662PubMedGoogle Scholar
  33. Liu Y, Zhang J, Zhang X, Xie S (2014b) Depth-related changes of sediment ammonia-oxidizing microorganisms in a high-altitude freshwater wetland. Appl Microbiol Biotechnol 98:5697–5707PubMedGoogle Scholar
  34. Liu J, Yu Z, Yao Q, Sui Y, Shi Y, Chu H et al (2019) Biogeographic distribution patterns of the archaeal communities across the black soil zone of Northeast China. Front Microbiol 10:23PubMedPubMedCentralGoogle Scholar
  35. Mackelprang R, Waldrop MP, DeAngelis KM, David MM, Chavarria KL, Blazewicz SJ et al (2011) Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480:368–371Google Scholar
  36. Martínez-Porchas M, Villalpando-Canchola E, Vargas-Albores F (2016) Significant loss of sensitivity and specificity in the taxonomic classification occurs when short 16S rRNA gene sequences are used. Heliyon 2:e00170PubMedPubMedCentralGoogle Scholar
  37. McKay LJ, Hatzenpichler R, Inskeep WP, Fields MW (2017) Occurrence and expression of novel methyl-coenzyme M reductase gene (mcrA) variants in hot spring sediments. Sci Rep 7:7252PubMedPubMedCentralGoogle Scholar
  38. Meng J, Xu J, Qin D, He Y, Xiao X, Wang F (2014) Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analysis. ISME J 8:650–659PubMedGoogle Scholar
  39. Mesa V, Gallego JLR, González-Gil R, Lauga B, Sánchez J, Méndez-Garcla C, Peláez AI (2017) Bacterial, archaeal, and eukaryotic diversity across distinct microhabitats in an acid mine drainage. Fron Microbiol 8:1756Google Scholar
  40. Nunoura T, Takaki Y, Kazama H, Hirai M, Ashi J, Imachi H, Takai K (2012) Microbial diversity in deep-sea methane seep sediments presented by SSU rRNA gene tag sequencing. Microbes Environ 27:381–390Google Scholar
  41. Olsen GJ, Lane DJ, Giovannoni SJ, Pace NR, Stahl DA (1986) Microbial ecology and evolution: a ribosomal RNA approach. Annu Rev Microbiol 40:337–365PubMedGoogle Scholar
  42. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Fangl JL, Buckler ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci USA 110:6548–6553PubMedGoogle Scholar
  43. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SSK, McCulle SL et al (2011) Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci USA 108(suppl l):4680–4687PubMedGoogle Scholar
  44. Schloss PD, Westcott SI, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541PubMedPubMedCentralGoogle Scholar
  45. Schloss PD, Jenior ML, Koumpouras CC, Westcott SL, Highlander SK (2016) Sequencing 16S rRNA gene fragments using the PacBio SMRT DNA sequencing system. PeerJ 4:e1869PubMedPubMedCentralGoogle Scholar
  46. Sinclair L, Osman OA, Bertilsson S, Eiler A (2015) Microbial community composition and diversity via 16S rRNA gene amplicons: evaluating the illumine platform. PLoS One 10:e0116955PubMedPubMedCentralGoogle Scholar
  47. Sollai M, Villanueva L, Hopmans E, Reichart GJ, Damsté JSS (2019) A combined lipidomic and 16S rRNA gene amplicon sequencing approach reveals archaeal sources of intact polar lipids in the stratified Black Sea water column. Geobiology 17:91–109PubMedGoogle Scholar
  48. Spang A, Saw JH, Jørgensen SL, Zarenba-Niedzwiedzka K, Martijin J, Lind AE et al (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521:173–179PubMedPubMedCentralGoogle Scholar
  49. Spang A, Caceres EF, Ettema TJG (2017) Genomic exploration of the diversity ecology and evolution of the archaeal domain of life. Science 357:3883Google Scholar
  50. Takahashi S, Tomita J, Nishioka K, Hisada T, Nishijima M (2014) Development of a prokaryotic universal primer for simultaneous analysis of bacteria and archaea using next-generation sequencing. PLoS One 9:e105592PubMedPubMedCentralGoogle Scholar
  51. Takai K, Horikoshi K (1999) Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152:1285–1297PubMedPubMedCentralGoogle Scholar
  52. Takai K, Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066–5072PubMedPubMedCentralGoogle Scholar
  53. Teske A, Sørensen KB (2008) Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME J 2:3–18PubMedGoogle Scholar
  54. Thijs S, Beeck MOP, Beckers B, Truyens S, Stevens V, Van Hamme JD, Weyens N, Vangronseld J (2017) Comparative evaluation of four bacteria-specific primer pairs for 16S rRNA gene surveys. Front Microbiol 8:494PubMedPubMedCentralGoogle Scholar
  55. Vavourakis CD, Ghai R, Rodriguez-Valera F, Sorokin DY, Tringe SG, Hugenholtz P, Muyzer G (2016) Metagenomic insights into the uncultured diversity and physiology of microbes in four hypersaline soda lake brines. Front Microbiol 7:211PubMedPubMedCentralGoogle Scholar
  56. Vetriani C, Jannasch HW, MacGregor BJ, Stahl DA, Reysenbach AL (1999) Population structure and phylogenetic characterization of marine benthic archaea in deep-sea sediments. Appl Environ Microbiol 65:4375–4384PubMedPubMedCentralGoogle Scholar
  57. Wang Y, Qian PY (2009) Conservative fragments in bacterial 16S rRNA genes and primers design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS ONE 4:e7401PubMedPubMedCentralGoogle Scholar
  58. Wei S, Cui H, Zhu Y, Lu Z, Pang S, Zhang S, Dong H, Su X (2018) Shifts of archaeal and methanogenic communities in response to permafrost thaw results in rising methane emissions and soil property changes. Extremophiles 22:447–459PubMedGoogle Scholar
  59. Yang B, Wang Y, Qian PY (2016a) Sensitivity and correlation of hypervariable regions in 16S rRNA genes in phylogenetic analysis. BMC Bioinformatics 17:135PubMedPubMedCentralGoogle Scholar
  60. Yang Y, Dai Y, Wu Z, Xie S, Liu Y (2016b) Temporal and spatial dynamics of archaeal communities in two freshwater lakes at different trophic status. Front Microbiol 7:451PubMedPubMedCentralGoogle Scholar
  61. You NH, Ashlock-Savage KN, Elshahed MS (2012) Phylogenetic diversities and community structure of members of the extremely halophilic archaea (Order Halobacteriales) in multiple saline sediments habitats. Appl Environ Microbiol 78:1332–1344Google Scholar
  62. Zhang J, Ding X, Guan R, Zhu C, Xu C, Zhu B et al (2018) Evaluation of different 16S rRNA gene V regions for exploring bacterial diversity in a eutrophic freshwater lake. Sci Total Environ 618:1254–1267PubMedGoogle Scholar
  63. Zheng W, Tsompana M, Ruscitto A, Sharma A, Genco R, Sun Y, Buck MJ (2015) An accurate and efficient experimental approach for characterization of the complex oral microbiota. Microbiome 3:48PubMedPubMedCentralGoogle Scholar
  64. Zhou HW, Li DF, Tam NFY, Jiang XT, Zhang H, Sheng HF et al (2011) BIPES, a cost-effective high-throughput method for assessing microbial diversity. ISME J 5:741–749PubMedGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Shiping Wei
    • 1
    • 2
    Email author
  • Hongpeng Cui
    • 2
  • Yuchen Zhang
    • 2
  • Xin Su
    • 2
  • Hailiang Dong
    • 1
  • Fang Chen
    • 3
  • Youhai Zhu
    • 4
  1. 1.State Key Laboratory of Biogeology and Environmental GeologyChina University of GeosciencesBeijingChina
  2. 2.School of Marine SciencesChina University of GeosciencesBeijingChina
  3. 3.Guangzhou Marine Geological SurveyGuangdongChina
  4. 4.Oil and Gas Survey, China Geological SurveyBeijingChina

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