Advertisement

Vertical Distribution of Bathyarchaeotal Communities in Mangrove Wetlands Suggests Distinct Niche Preference of Bathyarchaeota Subgroup 6

  • Jie Pan
  • Yulian Chen
  • Yongming Wang
  • Zhichao Zhou
  • Meng LiEmail author
Environmental Microbiology

Abstract

Bathyarchaeota is a diverse, abundant, and widespread archaeal phylum that may play an important role in global carbon cycling. The vertical distribution of Bathyarchaeota and environmental impact on bathyarchaeotal community in deep-sea and lake sediments are known; however, little information is available on Bathyarchaeota in eutrophic and brackish environments, such as mangrove wetlands. In the current study, we investigated the bathyarchaeotal community in the mangrove ecosystem of Futian Nature Reserve, Shenzhen. By slicing the profile into 2-cm layers from the surface to bottom, 110 sediment samples were obtained from three mangrove and three mud flat profiles. High-throughput sequencing of archaeal 16S rRNA genes, quantification of bathyarchaeotal 16S rRNA genes with optimized quantitative primers, and the ensuing statistical analyses revealed the vertical distribution of Bathyarchaeota in the mangrove ecosystem, indicating that Bathyarchaeota was the dominant archaeal phylum therein, with Bathyarchaeota subgroups 6, 8, 15, and 17 as the most abundant subgroups. The abundance of Bathyarchaeota was higher in the mangrove than in the mud flat and other oligotrophic or freshwater habitats. Total organic carbon (TOC) and nitric oxide were significantly correlated with the abundance of Bathyarchaeota, and pH was the major factor shaping the community composition. Further, the data suggested that Bathyarchaeota subgroup 6 preferentially dwelled in slightly acidic, high TOC, and subsurface environments, indicating a potentially distinct role in the global geochemical cycle. These findings expand the knowledge of the distribution and niche preference of Bathyarchaeota, emphasizing the need for continuous characterization of bathyarchaeotal subgroups.

Keywords

Bathyarchaeota Vertical distribution Subgroup 6 Primer Mangrove wetland Acidic 

Notes

Funding Information

This work was supported by the National Natural Science Foundation of China (grants no. 31600093, 41506163, 31622002, and 91851105); China Postdoctoral Science Foundation (grant no. 2016M602506); the Key Project of Department of Education of Guangdong Province (grant no. 2017KZDXM071); and the Science and Technology Innovation Committee of Shenzhen (grant no. JCYJ20170818091727570).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

248_2018_1309_MOESM1_ESM.pdf (11 mb)
Supplementary Figure 1 (PDF 11287 kb)
248_2018_1309_MOESM2_ESM.pdf (271 kb)
Supplementary Figure 2 (PDF 271 kb)
248_2018_1309_MOESM3_ESM.pdf (333 kb)
Supplementary Figure 3 (PDF 333 kb)
248_2018_1309_MOESM4_ESM.pdf (244 kb)
Supplementary Figure 4 (PDF 243 kb)
248_2018_1309_MOESM5_ESM.pdf (244 kb)
Supplementary Figure 5 (PDF 244 kb)
248_2018_1309_MOESM6_ESM.pdf (146 kb)
Supplementary Figure 6 (PDF 145 kb)
248_2018_1309_MOESM7_ESM.pdf (168 kb)
Supplementary Figure 7 (PDF 167 kb)
248_2018_1309_MOESM8_ESM.docx (163 kb)
ESM 1 (DOCX 162 kb)

References

  1. 1.
    Inagaki F, Suzuki M, Takai K, Oida H, Sakamoto T, Aoki K, Nealson KH, Horikoshi K (2003) Microbial communities associated with geological horizons in coastal subseafloor sediments from the sea of okhotsk. Appl Environ Microbiol 69:7224–7235CrossRefGoogle Scholar
  2. 2.
    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 analyses. ISME J 8:650–659.  https://doi.org/10.1038/ismej.2013.174 CrossRefPubMedGoogle Scholar
  3. 3.
    Lloyd KG, Schreiber L, Petersen DG, Kjeldsen KU, Lever MA, Steen AD, Stepanauskas R, Richter M, Kleindienst S, Lenk S, Schramm A, Jorgensen BB (2013) Predominant archaea in marine sediments degrade detrital proteins. Nature 496:215–218.  https://doi.org/10.1038/nature12033 CrossRefPubMedGoogle Scholar
  4. 4.
    Takai S, Henton MM, Picard JA, Guthrie AJ, Fukushi H, Sugimoto C (2001) Prevalence of virulent Rhodococcus equi in isolates from soil collected from two horse farms in South Africa and restriction fragment length polymorphisms of virulence plasmids in the isolates from infected foals, a dog and a monkey. Onderstepoort J Vet Res 68:105–110PubMedGoogle Scholar
  5. 5.
    Zhou Z, Meng H, Liu Y, Gu J-D, Li M (2017) Stratified bacterial and archaeal community in mangrove and intertidal wetland mudflats revealed by high throughput 16S rRNA gene sequencing. Front Microbiol 8:2148.  https://doi.org/10.3389/fmicb.2017.02148 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Vaksmaa A, van Alen TA, Ettwig KF, Lupotto E, Vale G, Jetten MSM, Luke C (2017) Stratification of diversity and activity of methanogenic and methanotrophic microorganisms in a nitrogen-fertilized Italian paddy soil. Front Microbiol 8:2127.  https://doi.org/10.3389/fmicb.2017.02127 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Xia X, Guo W, Liu H (2017) Basin scale variation on the composition and diversity of archaea in the Pacific Ocean. Front Microbiol 8:2057.  https://doi.org/10.3389/fmicb.2017.02057 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Inagaki F, Nunoura T, Nakagawa S, Teske A, Lever M, Lauer A, Suzuki M, Takai K, Delwiche M, Colwell FS, Nealson KH, Horikoshi K, D’Hondt S, Jorgensen BB (2006) Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments, on the Pacific Ocean Margin. Proc Natl Acad Sci U S A 103:2815–2820.  https://doi.org/10.1073/pnas.0511033103 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Seyler LM, McGuinness LM, Kerkhof LJ (2014) Crenarchaeal heterotrophy in salt marsh sediments. ISME J 8:1534–1543.  https://doi.org/10.1038/ismej.2014.15 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Li M, Jain S, Dick GJ (2016) Genomic and transcriptomic resolution of organic matter utilization among deep-sea bacteria in Guaymas Basin hydrothermal plumes. Front Microbiol 7:1125.  https://doi.org/10.3389/fmicb.2016.01125 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Kubo K, Lloyd KG, J FB, Amann R, Teske A, Knittel K (2012) Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments. ISME J 6:1949–1965.  https://doi.org/10.1038/ismej.2012.37 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–510.  https://doi.org/10.1038/35054051 CrossRefGoogle Scholar
  13. 13.
    Biddle JF, Lipp JS, Lever MA, Lloyd KG, Sorensen KB, Anderson R, Fredricks HF, Elvert M, Kelly TJ, Schrag DP, Sogin ML, Brenchley JE, Teske A, House CH, Hinrichs KU (2006) Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci U S A 103:3846–3851.  https://doi.org/10.1073/pnas.0600035103 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Lazar CS, Baker BJ, Seitz K, Hyde AS, Dick GJ, Hinrichs KU, Teske AP (2016) Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments. Environ Microbiol 18:1200–1211.  https://doi.org/10.1111/1462-2920.13142 CrossRefPubMedGoogle Scholar
  15. 15.
    He Y, Li M, Perumal V, Feng X, Fang J, Xie J, Sievert SM, Wang F (2016) Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nat Microbiol 1:16035.  https://doi.org/10.1038/nmicrobiol.2016.35 CrossRefGoogle Scholar
  16. 16.
    Evans PN, Parks DH, Chadwick GL, Robbins SJ, Orphan VJ, Golding SD, Tyson GW (2015) Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350:434–438.  https://doi.org/10.1126/science.aac7745 CrossRefGoogle Scholar
  17. 17.
    Zhou Z, Pan J, Wang F, Gu JD, Li M (2018) Bathyarchaeota: globally distributed metabolic generalists in anoxic environments. FEMS Microbiol Rev 42:639–655.  https://doi.org/10.1093/femsre/fuy023 CrossRefPubMedGoogle Scholar
  18. 18.
    Fillol Homs M (2017) Insights into the distribution and ecological role of members of the archaeal Phylum Bathyarchaeota. From the global to the local scale. Doctoral Thesis, Universitat de Girona, Universitat de GironaGoogle Scholar
  19. 19.
    Zhou Z, Zhang GX, Xu YB, Gu JD (2018) Successive transitory distribution of Thaumarchaeota and partitioned distribution of Bathyarchaeota from the Pearl River estuary to the northern South China Sea. Appl Microbiol Biotechnol 102:8035–8048.  https://doi.org/10.1007/s00253-018-9147-6 CrossRefPubMedGoogle Scholar
  20. 20.
    Yu T, Liang Q, Niu M, Wang F (2017) High occurrence of Bathyarchaeota (MCG) in the deep-sea sediments of South China Sea quantified using newly designed PCR primers. Environ Microbiol Rep 9:374–382.  https://doi.org/10.1111/1758-2229.12539 CrossRefPubMedGoogle Scholar
  21. 21.
    Fillol M, Auguet JC, Casamayor EO, Borrego CM (2016) Insights in the ecology and evolutionary history of the Miscellaneous Crenarchaeotic Group lineage. ISME J 10:665–677.  https://doi.org/10.1038/ismej.2015.143 CrossRefPubMedGoogle Scholar
  22. 22.
    Xiang X, Wang RC, Wang HM, Gong LF, Man BY, Xu Y (2017) Distribution of Bathyarchaeota communities across different terrestrial settings and their potential ecological functions. Sci Rep 7:ARTN 45028.  https://doi.org/10.1038/srep45028
  23. 23.
    Lazar CS, Biddle JF, Meador TB, Blair N, Hinrichs KU, Teske AP (2015) Environmental controls on intragroup diversity of the uncultured benthic archaea of the miscellaneous Crenarchaeotal group lineage naturally enriched in anoxic sediments of the White Oak River estuary (North Carolina, USA). Environ Microbiol 17:2228–2238.  https://doi.org/10.1111/1462-2920.12659 CrossRefPubMedGoogle Scholar
  24. 24.
    McKee KL (2011) Biophysical controls on accretion and elevation change in Caribbean mangrove ecosystems. Estuar Coast Shelf Sci 91:475–483.  https://doi.org/10.1016/j.ecss.2010.05.001 CrossRefGoogle Scholar
  25. 25.
    Donato DC, Kauffman JB, Murdiyarso D, Kurnianto S, Stidham M, Kanninen M (2011) Mangroves among the most carbon-rich forests in the tropics. Nat Geosci 4:293–297.  https://doi.org/10.1038/ngeo1123 CrossRefGoogle Scholar
  26. 26.
    Mcleod E, Chmura GL, Bouillon S, Salm R, Björk M, Duarte CM, Lovelock CE, Schlesinger WH, Silliman BR (2011) A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front Ecol Environ 9:552–560.  https://doi.org/10.1890/110004 CrossRefGoogle Scholar
  27. 27.
    Imchen M, Kumavath R, Barh D, Azevedo V, Ghosh P, Viana M, Wattam AR (2017) Searching for signatures across microbial communities: metagenomic analysis of soil samples from mangrove and other ecosystems. Sci Rep 7:8859.  https://doi.org/10.1038/s41598-017-09254-6 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Ikenaga M, Guevara R, Dean AL, Pisani C, Boyer JN (2010) Changes in community structure of sediment bacteria along the Florida Coastal Everglades marsh–mangrove–seagrass salinity gradient. Microb Ecol 59:284–295.  https://doi.org/10.1007/s00248-009-9572-2 CrossRefPubMedGoogle Scholar
  29. 29.
    Mendes LW, Tsai SM (2018) Distinct taxonomic and functional composition of soil microbiomes along the gradient forest-restinga-mangrove in southeastern Brazil. Antonie Van Leeuwenhoek 111:101–114.  https://doi.org/10.1007/s10482-017-0931-6 CrossRefPubMedGoogle Scholar
  30. 30.
    Bhattacharyya A, Majumder NS, Basak P, Mukherji S, Roy D, Nag S, Haldar A, Chattopadhyay D, Mitra S, Bhattacharyya M, Ghosh A (2015) Diversity and distribution of archaea in the mangrove sediment of Sundarbans. Archaea 2015:968582.  https://doi.org/10.1155/2015/968582 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Mendes LW, Taketani RG, Navarrete AA, Tsai SM (2012) Shifts in phylogenetic diversity of archaeal communities in mangrove sediments at different sites and depths in southeastern Brazil. Res Microbiol 163:366–377.  https://doi.org/10.1016/j.resmic.2012.05.005 CrossRefPubMedGoogle Scholar
  32. 32.
    Dias ACF, Dini-Andreote F, Taketani RG, Tsai SM, Azevedo JL, de Melo IS, Andreote FD (2011) Archaeal communities in the sediments of three contrasting mangroves. J Soils Sediments 11:1466–1476.  https://doi.org/10.1007/s11368-011-0423-7 CrossRefGoogle Scholar
  33. 33.
    Yan B, Hong K, Yu ZN (2006) Archaeal communities in mangrove soil characterized by 16S rRNA gene clones. J Microbiol 44:566–571PubMedGoogle Scholar
  34. 34.
    Ren H, Wu X, Ning T, Huang G, Wang J, Jian S, Lu H (2011) Wetland changes and mangrove restoration planning in Shenzhen Bay, Southern China. Landsc Ecol Eng 7:241–250.  https://doi.org/10.1007/s11355-010-0126-z CrossRefGoogle Scholar
  35. 35.
    Coolen MJL, Hopmans EC, Rijpstra WIC, Muyzer G, Schouten S, Volkman JK, Sinninghe Damsté JS (2004) Evolution of the methane cycle in Ace Lake (Antarctica) during the Holocene: response of methanogens and methanotrophs to environmental change. Org Geochem 35:1151–1167.  https://doi.org/10.1016/j.orggeochem.2004.06.009 CrossRefGoogle Scholar
  36. 36.
    Cheng YF, Mao SY, Liu JX, Zhu WY (2009) Molecular diversity analysis of rumen methanogenic Archaea from goat in eastern China by DGGE methods using different primer pairs. Lett Appl Microbiol 48:585–592.  https://doi.org/10.1111/j.1472-765X.2009.02583.x CrossRefPubMedGoogle Scholar
  37. 37.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336.  https://doi.org/10.1038/nmeth.f.303 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200.  https://doi.org/10.1093/bioinformatics/btr381 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596.  https://doi.org/10.1093/nar/gks1219 CrossRefPubMedGoogle Scholar
  40. 40.
    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461.  https://doi.org/10.1093/bioinformatics/btq461 CrossRefPubMedGoogle Scholar
  41. 41.
    Fillol M, Sanchez-Melsio A, Gich F, Borrego CM (2015) Diversity of Miscellaneous Crenarchaeotic Group archaea in freshwater karstic lakes and their segregation between planktonic and sediment habitats. FEMS Microbiol Ecol 91:fiv020.  https://doi.org/10.1093/femsec/fiv020 CrossRefPubMedGoogle Scholar
  42. 42.
    Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633–D642.  https://doi.org/10.1093/nar/gkt1244 CrossRefPubMedGoogle Scholar
  43. 43.
    Mount DW (2007) Using the Basic Local Alignment Search Tool (BLAST). CSH Protoc 2007:pdb top17.  https://doi.org/10.1101/pdb.top17 CrossRefPubMedGoogle Scholar
  44. 44.
    Welch BL (1947) The generalisation of student’s problems when several different population variances are involved. Biometrika 34:28–35PubMedGoogle Scholar
  45. 45.
    Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2011) vegan: community ecology package. R package version 117-118.https://CRAN.R-project.org/package=vegan
  46. 46.
    Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York http://ggplot2.org
  47. 47.
    Team RC (2018) R: A language and environment for statistical computing. https://www.R-project.org/
  48. 48.
    Faust K, Raes J (2016) CoNet app: inference of biological association networks using Cytoscape [version 2; referees: 2 approved]. F1000Research 5:1519.  https://doi.org/10.12688/f1000research.9050.2 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Zhou Z, Liu Y, Lloyd KG, Pan J, Yang Y, Gu J-D, Li M (2018) Genomic and transcriptomic insights into the ecology and metabolism of benthic archaeal cosmopolitan, Thermoprofundales (MBG-D archaea). ISME J.  https://doi.org/10.1038/s41396-018-0321-8
  50. 50.
    Rebollar EA, Sandoval-Castellanos E, Roessler K, Gaut BS, Alcaraz LD, Benítez M, Escalante AE (2017) Seasonal changes in a maize-based polyculture of Central Mexico reshape the co-occurrence networks of soil bacterial communities. Front Microbiol 8:2478.  https://doi.org/10.3389/fmicb.2017.02478 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Li W, Guan W, Chen H, Liao B, Hu J, Peng C, Rui J, Tian J, Zhu D, He Y (2016) Archaeal communities in the sediments of different mangrove stands at Dongzhaigang, China. J Soils Sediments 16:1995–2004.  https://doi.org/10.1007/s11368-016-1427-0 CrossRefGoogle Scholar
  52. 52.
    Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631.  https://doi.org/10.1073/pnas.0507535103 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Bååth E, Anderson TH (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–963.  https://doi.org/10.1016/S0038-0717(03)00154-8 CrossRefGoogle Scholar
  54. 54.
    Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351.  https://doi.org/10.1038/ismej.2010.58 CrossRefPubMedGoogle Scholar
  55. 55.
    Bengtson P, Sterngren AE, Rousk J (2012) Archaeal abundance across a pH gradient in an arable soil and its relationship to bacterial and fungal growth rates. Appl Environ Microbiol 78:5906–5911.  https://doi.org/10.1128/aem.01476-12 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Kemmitt SJ, Wright D, Goulding KWT, Jones DL (2006) pH regulation of carbon and nitrogen dynamics in two agricultural soils. Soil Biol Biochem 38:898–911.  https://doi.org/10.1016/j.soilbio.2005.08.006 CrossRefGoogle Scholar
  57. 57.
    Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10:2966–2978.  https://doi.org/10.1111/j.1462-2920.2008.01701.x CrossRefPubMedGoogle Scholar
  58. 58.
    Galand PE, Fritze H, Conrad R, Yrjälä K (2005) Pathways for methanogenesis and diversity of methanogenic archaea in three boreal peatland ecosystems. Appl Environ Microbiol 71:2195–2198.  https://doi.org/10.1128/AEM.71.4.2195-2198.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Dong K, Kim W-S, Tripathi BM, Adams J (2015) Generalized soil Thaumarchaeota community in weathering rock and saprolite. Microb Ecol 69:356–360.  https://doi.org/10.1007/s00248-014-0526-y CrossRefPubMedGoogle Scholar
  60. 60.
    Hu H-W, Zhang L-M, Yuan C-L, He J-Z (2013) Contrasting Euryarchaeota communities between upland and paddy soils exhibited similar pH-impacted biogeographic patterns. Soil Biol Biochem 64:18–27.  https://doi.org/10.1016/j.soilbio.2013.04.003 CrossRefGoogle Scholar
  61. 61.
    Glass C, Silverstein J, Oh J (1997) Inhibition of denitrification in activated sludge by nitrite. Water Environ Res 69:1086–1093.  https://doi.org/10.2175/106143097X125803 CrossRefGoogle Scholar
  62. 62.
    Almeida JS, Júlio SM, Reis MAM, Carrondo MJT (1995) Nitrite inhibition of denitrification by Pseudomonas fluorescens. Biotechnol Bioeng 46:194–201.  https://doi.org/10.1002/bit.260460303 CrossRefPubMedGoogle Scholar
  63. 63.
    Zhang W, Ding W, Yang B, Tian R, Gu S, Luo H, Qian PY (2016) Genomic and transcriptomic evidence for carbohydrate consumption among microorganisms in a cold seep brine pool. Front Microbiol 7:1825.  https://doi.org/10.3389/fmicb.2016.01825 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Harris RL, Lau MCY, Cadar A, Bartlett DH, Cason E, van Heerden E, Onstott TC (2018) Draft genome sequence of “Candidatus Bathyarchaeota” Archaeon BE326-BA-RLH, an uncultured denitrifier and putative anaerobic methanotroph from South Africa’s deep continental biosphere. Microbiol Resour Announc 7.  https://doi.org/10.1128/MRA.01295-18
  65. 65.
    Wei S, Cui H, He H, Hu F, Su X, Zhu Y (2014) Diversity and distribution of archaea community along a stratigraphic permafrost profile from Qinghai-Tibetan Plateau, China. Archaea 2014:240817.  https://doi.org/10.1155/2014/240817 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Meador TB, Bowles M, Lazar CS, Zhu C, Teske A, Hinrichs KU (2015) The archaeal lipidome in estuarine sediment dominated by members of the Miscellaneous Crenarchaeotal Group. Environ Microbiol 17:2441–2458.  https://doi.org/10.1111/1462-2920.12716 CrossRefPubMedGoogle Scholar
  67. 67.
    Li Q, Wang F, Chen Z, Yin X, Xiao X (2012) Stratified active archaeal communities in the sediments of Jiulong River estuary, China. Front Microbiol 3:311.  https://doi.org/10.3389/fmicb.2012.00311 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute for Advanced StudyShenzhen UniversityShenzhenPeople’s Republic of China
  2. 2.Key Laboratory of Optoelectronic Devices and Systems of Ministry of Education and Guangdong Province, College of Optoelectronic EngineeringShenzhen UniversityShenzhenPeople’s Republic of China
  3. 3.College of Life Sciences and OceanographyShenzhen UniversityShenzhenPeople’s Republic of China

Personalised recommendations