Environmental factors shaping the archaeal community structure and ether lipid distribution in a subtropic river and estuary, China

  • Wenting Guo
  • Wei Xie
  • Xueying Li
  • Peng Wang
  • Anyi Hu
  • Chuanlun L. Zhang
Environmental biotechnology

Abstract

Archaea are widespread and abundant in aquatic and terrestrial habitats and play fundamental roles in global biogeochemical cycles. Archaeal lipids, such as isoprenoid glycerol diakyl glycerol tetraethers (iGDGTs), are important biomarkers tracing changes in archaeal community structure and biogeochemical processes in nature. However, the linkage between the archaeal populations and the GDGT distribution in the natural environment is poorly examined, which hindered the application and interpretation of GDGT-based climate or environmental proxies. We addressed this question by investigating changes in archaeal lipid composition and community structure in the context of environmental variables along the subtropical Jiulong River Watershed (JRW) and Jiulong River Estuary (JRE) in southern China. The results showed that both the archaeal cells and the polar GDGTs (P-GDGTs) in the JRW and JRE were mostly autochthonous rather than exogenous input from surrounding soils. We further found that only five (Methanobacteriales, Ca. Bathyarchaeota, Marine Benthic Groups A (MBGA), Marine Benthic Groups B (MBGB), and Marine Benthic Groups D (MBGD)) out of sixteen lineages showed significant impacts on the composition of P-GDGTs, suggesting the significant contribution of those archaea to the changes of P-GDGT compositions. Salinity and total phosphorus (TP) showed significant impact on the distribution of both genetic and P-GDGTs compositions of archaea; whereas, sand and silt contents only had significant impact on the P-GDGTs. MBGD archaea, which occur widely in marine sediments, showed positive correlations with P-TEX86 in the JRW and JRE, suggesting that uncultivated MBGD might also contribute to the variations in TEX86 signals in marine sediments. This study provided insight into the sources of P-GDGTs and the factors controlling their distributions in river-dominated continental margins, which has relevance to applications of GDGT-based proxies in paleoclimate studies.

Keywords

Archaea TEX86 P-GDGTs Jiulong River Watershed Jiulong River Estuary 

Supplementary material

253_2017_8595_MOESM1_ESM.pdf (1001 kb)
ESM 1(PDF 1000 kb)

References

  1. Auguet JC, Barberan A, Casamayor EO (2010) Global ecological patterns in uncultured archaea. ISME J 4(2):182–190. https://doi.org/10.1038/ismej.2009.109 CrossRefPubMedGoogle Scholar
  2. Bano N, Ruffin S, Ransom B, Hollibaugh JT (2004) Phylogenetic composition of Arctic Ocean archaeal assemblages and comparison with Antarctic assemblages. Appl Environ Microbiol 70(2):781–789. https://doi.org/10.1128/aem.70.2.781-789.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Becker KW, Elling FJ, Yoshinaga MY, Söllinger A, Urich T, Hinrichs K-U (2016) Unusual butane- and pentanetriol-based tetraether lipids in Methanomassiliicoccus luminyensis, a representative of the seventh order of methanogens. Appl Environ Microbiol 82(15):4505–4516. https://doi.org/10.1128/AEM.00772-16 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5(219):10.3389. https://doi.org/10.3389/fmicb.2014.00219 Google Scholar
  5. 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 C. H, Hinrichs KU (2006) Heterotrophic archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci U S A 103(10):3846–3851. https://doi.org/10.1073/pnas.0600035103 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Blumenberg M, Seifert R, Reitner J, Pape T, Michaelis W (2004) Membrane lipid patterns typify distinct anaerobic methanotrophic consortia. Proc Natl Acad Sci U S A 101(30):11111–11116. https://doi.org/10.1073/pnas.0401188101 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Boyd ES, Pearson A, Pi Y, Li WJ, Zhang YG, He L, Zhang CL, Geesey GG (2011) Temperature and pH controls on glycerol dibiphytanyl glycerol tetraether lipid composition in the hyperthermophilic crenarchaeon Acidilobus sulfurireducens. Extremophiles 15(1):59–65. https://doi.org/10.1007/s00792-010-0339-y CrossRefPubMedGoogle Scholar
  8. Ter Braak C. and Smilauer P. (2002). Canoco for Windows version 4.5, Biometris-Plant Research International, Wageningen.Google Scholar
  9. Cao H, Zhang W, Wang Y, Qian P-Y (2015) Microbial community changes along the active seepage site of one cold seep in the Red Sea Front Microbiol 6. doi:https://doi.org/10.3389/fmicb.2015.00739.
  10. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chen G-C, Ye Y, Lu C-Y (2007) Changes of macro-benthic faunal community with stand age of rehabilitated Kandelia candel mangrove in Jiulongjiang Estuary, China. Ecol Eng 31(3):215–224. https://doi.org/10.1016/j.ecoleng.2007.07.002 CrossRefGoogle Scholar
  12. Chen N, Peng B, Hong H, Turyaheebwa N, Cui S, Mo X (2013) Nutrient enrichment and N:P ratio decline in a coastal bay–river system in southeast China: the need for a dual nutrient (N and P) management strategy. Ocean Coast Manag 81:7–13. https://doi.org/10.1016/j.ocecoaman.2012.07.013 CrossRefGoogle Scholar
  13. Chevalier N, Bouloubassi I, Stadnitskaia A, Taphanel M-H, Damsté JSS (2014) Lipid biomarkers for anaerobic oxidation of methane and sulphate reduction in cold seep sediments of Nyegga pockmarks (Norwegian margin): discrepancies in contents and carbon isotope signatures. Geo-Mar Lett 34(2–3):269–280CrossRefGoogle Scholar
  14. De Rosa M, Gambacorta A, Gliozzi A (1986) Structure, biosynthesis, and physicochemical properties of archaebacterial lipids. Microbiol Rev 50(1):70. https://doi.org/10.1007/s00367-014-0363-5 PubMedPubMedCentralGoogle Scholar
  15. DeLong EF (1998) Everything in moderation: archaea as ‘non-extremophiles’. Curr Opin Genet Dev 8(6):649–654. https://doi.org/10.1016/S0959-437X(98)80032-4 CrossRefPubMedGoogle Scholar
  16. Elling F. J., Könneke M., Nicol G. W., Stieglmeier M., Bayer B., Spieck E., de la Torre J. R., Becker K. W., Thomm M. and Prosser J. I. (2017). Chemotaxonomic characterisation of the thaumarchaeal lipidome. Environ Microbiol 19(7): 2681–2700.Google Scholar
  17. Harvey HR, Fallon RD, Patton JS (1986) The effect of organic matter and oxygen on the degradation of bacterial membrane lipids in marine sediments. Geochim Cosmochim Acta 50(5):795–804. https://doi.org/10.1016/0016-7037(86)90355-8 CrossRefGoogle Scholar
  18. Hopmans E. C., Schouten S., Pancost R. D., van der Meer M. T. and Sinninghe Damsté J. S. (2000). Analysis of intact tetraether lipids in archaeal cell material and sediments by high performance liquid chromatography/atmospheric pressure chemical ionization mass spectrometry. Rapid Commun Mass Spectrom 14(7): 585–589 doi: https://doi.org/10.1002/(SICI)1097-0231(20000415)14:7<585::AID-RCM913>3.0.CO;2-N.
  19. Hu A, Hou L, Yu CP (2015) Biogeography of planktonic and benthic archaeal communities in a subtropical eutrophic estuary of China. Microb Ecol 70(2):322–335. https://doi.org/10.1007/s00248-015-0597-4 CrossRefPubMedGoogle Scholar
  20. Imachi H, Aoi K, Tasumi E, Saito Y, Yamanaka Y, Saito Y, Yamaguchi T, Tomaru H, Takeuchi R, Morono Y (2011) Cultivation of methanogenic community from subseafloor sediments using a continuous-flow bioreactor. ISME J 5(12):1913–1925. https://doi.org/10.1038/ismej.2011.64 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Inagaki F, Nunoura T, Nakagawa S, Teske A, Lever M, Lauer A, Suzuki M, Takai K, Delwiche M, Colwell FS (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(8):2815–2820. https://doi.org/10.1073/pnas.0511033103 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Jiang L, Zheng Y, Chen J, Xiao X, Wang F (2011) Stratification of archaeal communities in shallow sediments of the Pearl River Estuary, Southern China. Antonie Van Leeuwenhoek 99(4):739–751. https://doi.org/10.1007/s10482-011-9548-3 CrossRefPubMedGoogle Scholar
  23. Kerou M, Schleper C (2016) Nitrososphaera. Bergey’s manual of systematics of archaea and bacteria. doi:https://doi.org/10.1002/9781118960608.gbm01294
  24. Kim J.-H., Van der Meer J., Schouten S., Helmke P., Willmott V., Sangiorgi F., Koç N., Hopmans E. C. and Sinninghe Damsté J. S. (2010). New indices and calibrations derived from the distribution of crenarchaeal isoprenoid tetraether lipids: implications for past sea surface temperature reconstructions. Geochim Cosmochim Acta 74(16): 4639–4654 doi: https://doi.org/10.1016/j.gca.2010.05.027.
  25. Kim J-H, Zell C, Moreira-Turcq P, Pérez MA, Abril G, Mortillaro J-M, Weijers JW, Meziane T, Damsté JSS (2012) Tracing soil organic carbon in the lower Amazon River and its tributaries using GDGT distributions and bulk organic matter properties. Geochim Cosmochim Acta 90:163–180. https://doi.org/10.1016/j.gca.2012.05.014 CrossRefGoogle Scholar
  26. Langworthy TA, Pond JL (1986) Archaebacterial ether lipids and chemotaxonomy. Syst Appl Microbiol 7(2–3):253–257. https://doi.org/10.1016/S0723-2020(86)80015-7 CrossRefGoogle Scholar
  27. Li F, Zhang CL, Wang S, Chen Y, Sun C, Dong H, Li W, Klotz MG, Hedlund BP (2014) Production of branched tetraether lipids in Tibetan hot springs: a possible linkage to nitrite reduction by thermotolerant or thermophilic bacteria? Chem Geol 386:209–217. https://doi.org/10.1016/j.chemgeo.2014.08.015 CrossRefGoogle Scholar
  28. Li X, Zheng F, Chen Y, Guo W, Zhang T, Hu A, Yu C, Zhang C (2016) The spatial distribution of archaeal lipids in a mesoscale subtropical watershed, Southeast China. Sci China Earth Sci 59(7):1317–1328. https://doi.org/10.1007/s11430-016-5303-y CrossRefGoogle Scholar
  29. Li F, Zheng F, Wang Y, Liu W, Zhang C (2017) Thermoplasmatales and methanogens: potential association with the crenarchaeol production in Chinese soils. Front Microbiol 8:1200. https://doi.org/10.3389/fmicb.2017.01200 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lincoln SA, Wai B, Eppley JM, Church MJ, Summons RE, DeLong EF (2014) Planktonic Euryarchaeota are a significant source of archaeal tetraether lipids in the ocean. Proc Natl Acad Sci U S A 111(27):9858–9863. https://doi.org/10.1073/pnas.1409439111 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Lipp JS, Morono Y, Inagaki F, Hinrichs KU (2008) Significant contribution of archaea to extant biomass in marine subsurface sediments. Nature 454(7207):991–994. https://doi.org/10.1038/nature07174 CrossRefPubMedGoogle Scholar
  32. Macalady JL, Vestling MM, Baumler D, Boekelheide N, Kaspar CW, Banfield JF (2004) Tetraether-linked membrane monolayers in Ferroplasma spp: a key to survival in acid. Extremophiles 8(5):411–419. https://doi.org/10.1007/s00792-004-0404-5 CrossRefPubMedGoogle Scholar
  33. Meador TB, Bowles M, Lazar CS, Zhu C, Teske A, Hinrichs KU (2014) The archaeal lipidome in estuarine sediment dominated by members of the Miscellaneous Crenarchaeotal Group. Environ Microbiol 17(7):2441–2458. https://doi.org/10.1111/1462-2920.12716. CrossRefGoogle Scholar
  34. Morii H, Eguchi T, Nishihara M, Kakinuma K, König H, Koga Y (1998) A novel ether core lipid with H-shaped C80-isoprenoid hydrocarbon chain from the hyperthermophilic methanogen Methanothermus fervidus. BBA-Mol Cell Biol L 1390(3):339–345. https://doi.org/10.1016/S0005-2760(97)00183-5 Google Scholar
  35. Nichols PD, Franzmann PD (1992) Unsaturated diether phospholipids in the Antarctic methanogen Methanococcoides burtonii. FEMS Microbiol Lett 98(1–3):205–208CrossRefGoogle Scholar
  36. Nunoura T, Takaki Y, Shimamura S, Kakuta J, Kazama H, Hirai M, Masui N, Tomaru H, Morono Y, Imachi H (2016) Variance and potential niche separation of microbial communities in subseafloor sediments off Shimokita Peninsula, Japan. Environ Microbiol 18(6):1889–1906. https://doi.org/10.1111/1462-2920.13096 CrossRefPubMedGoogle Scholar
  37. Omoregie EO, Mastalerz V, De Lange G, Straub KL, Kappler A, Røy H, Stadnitskaia A, Foucher J-P, Boetius A (2008) Biogeochemistry and community composition of iron-and sulfur-precipitating microbial mats at the Chefren Mud Volcano (Nile Deep Sea Fan, Eastern Mediterranean). Appl Environ Microbiol 74(10):3198–3215. https://doi.org/10.1128/AEM.01751-07 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Orphan VJ, House CH, Hinrichs K-U, McKeegan KD, DeLong EF (2002) Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc Natl Acad Sci U S A 99(11):7663–7668. https://doi.org/10.1073/pnas.072210299 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Pancost R, Hopmans E, Damsté JS (2001) Archaeal lipids in Mediterranean cold seeps: molecular proxies for anaerobic methane oxidation. Geochim Cosmochim Acta 65(10):1611–1627. https://doi.org/10.1016/S0016-7037(00)00562-7 CrossRefGoogle Scholar
  40. Panke-Buisse K, Lee S, Kao-Kniffin J (2017) Cultivated sub-populations of soil microbiomes retain early flowering plant trait. Microb Ecol 73(2):394–403. https://doi.org/10.1007/s00248-016-0846-1 CrossRefPubMedGoogle Scholar
  41. Pearson A, Huang ZY, Ingalls AE, Romanek CS, Wiegel J, Freeman KH, Smittenberg RH, Zhang CL (2004) Nonmarine crenarchaeol in Nevada hot springs. Appl Environ Microbiol 70(9):5229–5237. https://doi.org/10.1128/AEM.70.9.5229-5237.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Peterse F, Moy C, Eglinton T (2015) A laboratory experiment on the behaviour of soil-derived core and intact polar GDGTs in aquatic environments. Biogeosciences 12(4):933. https://doi.org/10.5194/bg-12-933-2015 CrossRefGoogle Scholar
  43. Petsch S, Eglinton T, Edwards K (2001) 14C-dead living biomass: evidence for microbial assimilation of ancient organic carbon during shale weathering. Science 292(5519):1127–1131. https://doi.org/10.1126/science.1058332 CrossRefPubMedGoogle Scholar
  44. Pitcher A, Rychlik N, Hopmans EC, Spieck E, Rijpstra WI, Ossebaar J, Schouten S, Wagner M, Sinninghe Damsté JS (2010) Crenarchaeol dominates the membrane lipids of Candidatus Nitrososphaera gargensis, a thermophilic group I.1b Archaeon. ISME J 4(4):542–552. https://doi.org/10.1038/ismej.2009.138 CrossRefPubMedGoogle Scholar
  45. Powers LA, Werne JP, Johnson TC, Hopmans EC, Sinninghe Damsté JS, Schouten S (2004) Crenarchaeotal membrane lipids in lake sediments: a new paleotemperature proxy for continental paleoclimate reconstruction? Geology 32(7):613–616. https://doi.org/10.1130/G20434.1 CrossRefGoogle Scholar
  46. Powers LA, Werne JP, Vanderwoude AJ, Sinninghe Damsté JS, Hopmans EC, Schouten S (2010) Applicability and calibration of the TEX86 paleothermometer in lakes. Org Geochem 41(4):404–413. https://doi.org/10.1016/j.orggeochem.2009.11.009 CrossRefGoogle Scholar
  47. Qin W, Carlson LT, Armbrust EV, Devol AH, Moffett JW, Stahl DA, Ingalls AE (2015) Confounding effects of oxygen and temperature on the TEX86 signature of marine Thaumarchaeota. Proc Natl Acad Sci 112(35):10979–10984. https://doi.org/10.1073/pnas.1501568112 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Qin W, Martens-Habbena W, Kobelt JN, Stahl DA (2016) Candidatus nitrosopumilus. Bergey's manual of systematics of archaea and bacteria. doi:https://doi.org/10.1002/9781118960608.gbm01290.
  49. Rossel PE, Lipp JS, Fredricks HF, Arnds J, Boetius A, Elvert M, Hinrichs K-U (2008) Intact polar lipids of anaerobic methanotrophic archaea and associated bacteria. Org Geochem 39(8):992–999. https://doi.org/10.1016/j.orggeochem.2008.02.021 CrossRefGoogle Scholar
  50. Rossel PE, Elvert M, Ramette A, Boetius A, Hinrichs K-U (2011) Factors controlling the distribution of anaerobic methanotrophic communities in marine environments: evidence from intact polar membrane lipids. Geochim Cosmochim Acta 75(1):164–184. https://doi.org/10.1016/j.gca.2010.09.031 CrossRefGoogle Scholar
  51. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. https://doi.org/10.1128/AEM.01541-09 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Schouten S, Hopmans EC, Schefuß E, Sinninghe Damsté JS (2002) Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures? Earth Planet Sci Lett 204(1):265–274. https://doi.org/10.1016/S0012-821X(02)00979-2 CrossRefGoogle Scholar
  53. Schouten S, van der Meer MT, Hopmans EC, Rijpstra WI, Reysenbach AL, Ward DM, Sinninghe Damsté JS (2007) Archaeal and bacterial glycerol dialkyl glycerol tetraether lipids in hot springs of yellowstone national park. Appl Environ Microbiol 73(19):6181–6191. https://doi.org/10.1128/AEM.00630-07 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Schouten S, Hopmans EC, Sinninghe Damsté JS (2013) The organic geochemistry of glycerol dialkyl glycerol tetraether lipids: a review. Org Geochem 54:19–61. https://doi.org/10.1016/j.orggeochem.2012.09.006 CrossRefGoogle Scholar
  55. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504. https://doi.org/10.1101/gr.1239303 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Shevenell AE, Ingalls AE, Domack EW, Kelly C (2011) Holocene Southern Ocean surface temperature variability west of the Antarctic Peninsula. Nature 470(7333):250–254. https://doi.org/10.1038/nature09751 CrossRefPubMedGoogle Scholar
  57. Singh D, Takahashi K, Adams JM (2012) Elevational patterns in archaeal diversity on Mt. Fuji. PLoS One 7(9):e44494. https://doi.org/10.1371/journal.pone.0044494 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Sinninghe Damsté JS, Rijpstra WI, Hopmans EC, Jung MY, Kim JG, Rhee SK, Stieglmeier M, Schleper C (2012) Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids of group I.1a and I.1b thaumarchaeota in soil. Appl Environ Microbiol 78(19):6866–6874. https://doi.org/10.1128/AEM.01681-12 CrossRefPubMedCentralGoogle Scholar
  59. Sluijs A, Schouten S, Pagani M, Woltering M, Brinkhuis H, Sinninghe Damste JS, Dickens GR, Huber M, Reichart GJ, Stein R, Matthiessen J, Lourens LJ, Pedentchouk N, Backman J, Moran K, Expedition S (2006) Subtropical Arctic Ocean temperatures during the Palaeocene/Eocene thermal maximum. Nature 441(7093):610–613. https://doi.org/10.1038/nature04668 CrossRefPubMedGoogle Scholar
  60. Sprott G, Dicaire C, Patel G (1994) The ether lipids of Methanosarcina mazei and other Methanosarcina species, compared by fast atom bombardment mass spectrometry. Can J Microbiol 40(10):837–843. https://doi.org/10.1139/m94-133 CrossRefGoogle Scholar
  61. Sprott GD, Agnew BJ, Patel GB (1997) Structural features of ether lipids in the archaeobacterial thermophiles Pyrococcus furiosus, Methanopyrus kandleri, Methanothermus fervidus, and Sulfolobus acidocaldarius. Can J Microbiol 43(5):467–476. https://doi.org/10.1139/m97-066 CrossRefGoogle Scholar
  62. Sprott GD, Brisson J-R, Dicaire CJ, Pelletier AK, Deschatelets LA, Krishnan L, Patel GB (1999) A structural comparison of the total polar lipids from the human archaea Methanobrevibacter smithii and Methanosphaera stadtmanae and its relevance to the adjuvant activities of their liposomes. BBA-Mol Cell Biol L 1440(2):275–288. https://doi.org/10.1016/S1388-1981(99)00130-4 CrossRefGoogle Scholar
  63. Sturt HF, Summons RE, Smith K, Elvert M, Hinrichs KU (2004) Intact polar membrane lipids in prokaryotes and sediments deciphered by high-performance liquid chromatography/electrospray ionization multistage mass spectrometry-new biomarkers for biogeochemistry and microbial ecology. Rapid Commun Mass Spectrom 18(6):617–628Google Scholar
  64. 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(3):810–818. https://doi.org/10.1111/j.1462-2920.2007.01506.x CrossRefPubMedGoogle Scholar
  65. Valentine DL (2007) Adaptations to energy stress dictate the ecology and evolution of the archaea. Nat Rev Microbiol 5(4):316–323. https://doi.org/10.1038/nrmicro1619 CrossRefPubMedGoogle Scholar
  66. Vetriani C, Jannasch HW, MacGregor BJ, Stahl DA, Reysenbach A-L (1999) Population structure and phylogenetic characterization of marine benthic archaea in deep-sea sediments. Appl Environ Microbiol 65(10):4375–4384PubMedPubMedCentralGoogle Scholar
  67. van de Vossenberg JL, Driessen AJ, Konings WN (1998) The essence of being extremophilic: the role of the unique archaeal membrane lipids. Extremophiles 2(3):163–170. https://doi.org/10.1007/s007920050056 CrossRefPubMedGoogle Scholar
  68. Wakeham SG, Lewis CM, Hopmans EC, Schouten S, Damsté JSS (2003) Archaea mediate anaerobic oxidation of methane in deep euxinic waters of the Black Sea. Geochim Cosmochim Acta 67(7):1359–1374. https://doi.org/10.1016/S0016-7037(02)01220-6 CrossRefGoogle Scholar
  69. Wang P, Li T, Hu A, Wei Y, Guo W, Jiao N, Zhang C (2010) Community structure of archaea from deep-sea sediments of the South China Sea. Microb Ecol 60(4):796–806. https://doi.org/10.1007/s00248-010-9746-y CrossRefPubMedGoogle Scholar
  70. Wang J-T, Cao P, Hu H-W, Li J, Han L-L, Zhang L-M, Zheng Y-M, He J-Z (2015a) Altitudinal distribution patterns of soil bacterial and archaeal communities along Mt. Shegyla on the Tibetan Plateau. Microb Ecol 69(1):135–145. https://doi.org/10.1016/S0016-7037(02)01220-6. CrossRefPubMedGoogle Scholar
  71. Wang J-X, Wei Y, Wang P, Hong Y, Zhang CL (2015b) Unusually low TEX 86 values in the transitional zone between Pearl River estuary and coastal South China Sea: impact of changing archaeal community composition. Chem Geol 402:18–29. https://doi.org/10.1016/j.chemgeo.2015.03.002 CrossRefGoogle Scholar
  72. White D, Davis W, Nickels J, King J, Bobbie R (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40(1):51–62. https://doi.org/10.1007/BF00388810 CrossRefPubMedGoogle Scholar
  73. Wu W, Ruan J, Ding S, Zhao L, Xu Y, Yang H, Ding W, Pei Y (2014) Source and distribution of glycerol dialkyl glycerol tetraethers along lower Yellow River-estuary–coast transect. Mar Chem 158:17–26. https://doi.org/10.1016/j.marchem.2013.11.006 CrossRefGoogle Scholar
  74. Xie W, Zhang CL, Wang J, Chen Y, Zhu Y, de la Torre JR, Dong H, Hartnett HE, Hedlund BP, Klotz MG (2014a) Distribution of ether lipids and composition of the archaeal community in terrestrial geothermal springs: impact of environmental variables. Environ Microbiol 17:1600–1614. https://doi.org/10.1111/1462-2920.12595 CrossRefPubMedGoogle Scholar
  75. Xie W, Zhang CL, Zhou X, Wang P (2014b) Salinity-dominated change in community structure and ecological function of archaea from the lower Pearl River to coastal South China Sea. Appl Microbiol Biotechnol 98(18):7971–7982. https://doi.org/10.1007/s00253-014-5838-9 CrossRefPubMedGoogle Scholar
  76. Xie W, Zhang CL, Ma C (2015) Temporal variation in community structure and lipid composition of Thaumarchaeota from subtropical soil: insight into proposing a new soil pH proxy. Org Geochem 83:54–64. https://doi.org/10.1016/j.orggeochem.2015.02.009. CrossRefGoogle Scholar
  77. Yang G, Zhang CL, Xie S, Chen Z, Gao M, Ge Z, Yang Z (2013) Microbial glycerol dialkyl glycerol tetraethers from river water and soil near the three gorges dam on the Yangtze River. Org Geochem 56:40–50. https://doi.org/10.1016/j.orggeochem.2012.11.014 CrossRefGoogle Scholar
  78. Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89(6):670–679. https://doi.org/10.1002/bit.20347 CrossRefPubMedGoogle Scholar
  79. Zell C, Kim J-H, Hollander D, Lorenzoni L, Baker P, Silva CG, Nittrouer C, Damsté JSS (2014) Sources and distributions of branched and isoprenoid tetraether lipids on the Amazon shelf and fan: implications for the use of GDGT-based proxies in marine sediments. Geochim Cosmochim Acta 139:293–312. https://doi.org/10.1126/science.1246172 CrossRefGoogle Scholar
  80. Zhang YG, Zhang CL, Liu X-L, Li L, Hinrichs K-U, Noakes JE (2011) Methane index: a tetraether archaeal lipid biomarker indicator for detecting the instability of marine gas hydrates. Earth Planet Sci Lett 307(3):525–534. https://doi.org/10.1016/j.epsl.2011.05.031 CrossRefGoogle Scholar
  81. Zhang YG, Pagani M, Liu Z (2014) A 12-million-year temperature history of the tropical Pacific Ocean. Science 344(6179):84–87CrossRefPubMedGoogle Scholar
  82. Zhang YG, Pagani M, Wang Z (2016) Ring index: a new strategy to evaluate the integrity of TEX86 paleothermometry. Paleoceanography. https://doi.org/10.1002/2015PA002848
  83. Zhu C, Weijers JWH, Wagner T, Pan J-M, Chen J-F, Pancost RD (2011) Sources and distributions of tetraether lipids in surface sediments across a large river-dominated continental margin. Org Geochem 42(4):376–386. https://doi.org/10.1016/j.orggeochem.2011.02.002 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Wenting Guo
    • 1
    • 2
    • 3
  • Wei Xie
    • 1
    • 3
  • Xueying Li
    • 1
  • Peng Wang
    • 1
  • Anyi Hu
    • 3
  • Chuanlun L. Zhang
    • 4
  1. 1.State Key Lab of Marine GeologyTongji UniversityShanghaiChina
  2. 2.School of Marine SciencesNanjing University of Information Science and TechnologyNanjingChina
  3. 3.Key Lab of Urban Pollutant Conversion, Institute of Urban EnvironmentChinese Academy of SciencesXiamenChina
  4. 4.Department of Ocean Science and EngineeringSouthern University of Science and TechnologyShenzhenChina

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