Planktonic euryarchaeota are a significant source of archaeal tetraether lipids in the ocean

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 27, 2014, Pages 9858-9863

  Lincoln, Sara A ^a,b,e   Wai, Brenner ^b,c   Eppley, John M ^b,d   Church, Matthew J ^b,c   Summons, Roger E ^a   DeLong, Edward F ^b,c,d  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c UNIVERSITY OF HAWAII   (United States)

^d Massachusetts Institute of Technology Cambridge   (United States)

^e PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Environmental genomics; Euryarchaea; Glycerol dialkyl glycerol tetraether; Oceanography

Indexed keywords

CRENARCHAEOL; ETHER LIPID; MEMBRANE LIPID; NUCLEIC ACID; ORGANIC MATTER; RIBOSOME RNA; UNCLASSIFIED DRUG;

ARTICLE; BIOGEOCHEMICAL CYCLE; CLADISTICS; CONTROLLED STUDY; EURYARCHAEOTA; LIPID ANALYSIS; LIPID COMPOSITION; LIPOGENESIS; MARINE SPECIES; METAGENOMICS; NONHUMAN; NUCLEIC ACID ANALYSIS; PHYTOPLANKTON; PREVALENCE; PRIORITY JOURNAL; STRATIFICATION;

ENVIRONMENTAL GENOMICS; EURYARCHAEA; GLYCEROL DIALKYL GLYCEROL TETRAETHER; OCEANOGRAPHY; TEX86 INDEX;

ARCHAEA; BASE SEQUENCE; BIOLOGICAL MARKERS; DNA PRIMERS; ECOLOGY; ETHERS; LIPIDS; METAGENOMICS; PACIFIC OCEAN; PLANKTON; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84903978319     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1409439111     Document Type: Article

References (82)

1. DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89(12):5685-5689.
2. Fuhrman JA, McCallum K, Davis AA (1992) Novel major archaebacterial group from marine plankton. Nature 356(6365):148-149.
3. DeLong EF (2003) Oceans of archaea. Am Soc Microbiol News 69(10):503-511.
4. Schouten S, Hopmans E, Sinninghe Damsté J (2013) The organic geochemistry of glycerol dialkyl glycerol tetraether lipids: A review. Org Geochem 54:19-61.
5. Sinninghe Damsté JS, et al. (2002) Distribution of membrane lipids of planktonic Crenarchaeota in the Arabian Sea. Appl Environ Microbiol 68(6):2997-3002.
6. Wuchter C, Schouten S, Boschker HTS, Sinninghe Damsté JS (2003) Bicarbonate uptake by marine Crenarchaeota. FEMS Microbiol Lett 219(2):203-207. (Pubitemid 36302598)
7. Pearson A, McNichol AP, Benitez-Nelson BC, Hayes JM, Eglinton TI (2001) Origins of lipid biomarkers in Santa Monica Basin surface sediment: A case study using compound-specific Δ14C analysis. Geochim Cosmochim Acta 65(18):3123-3137. (Pubitemid 32974570)
8. Ingalls AE, et al. (2006) Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc Natl Acad Sci USA 103(17):6442-6447.
9. 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(1-2):265-274. (Pubitemid 35389745)
10. Hopmans EC, et al. (2004) A novel proxy for terrestrial organic matter in sediments based on branched and isoprenoid tetraether lipids. Earth Planet Sci Lett 224(1-2):107-116. (Pubitemid 38964592)
11. Kuypers MM, et al. (2001) Massive expansion of marine archaea during a mid-Cretaceous oceanic anoxic event. Science 293(5527):92-95.
12. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic Crenarchaeota: Proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6(3):245-252. (Pubitemid 351256319)
13. Könneke M, et al. (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437(7058):543-546. (Pubitemid 41613550)
14. 2O produced by marine ammonia-oxidizing archaea. Science 333(6047):1282-1285.
15. Metcalf WW, et al. (2012) Synthesis of methylphosphonic acid by marine microbes: A source for methane in the aerobic ocean. Science 337(6098):1104-1107.
16. Schouten S, et al. (2008) Intact membrane lipids of "Candidatus Nitrosopumilus maritimus," a cultivated representative of the cosmopolitan mesophilic group I Crenarchaeota. Appl Environ Microbiol 74(8):2433-2440. (Pubitemid 351555455)
17. Damsté JS, Schouten S, Hopmans EC, van Duin AC, Geenevasen JA (2002) Crenarchaeol: The characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota. J Lipid Res 43(10):1641-1651. (Pubitemid 35168278)
18. de la Torre JR, Walker CB, Ingalls AE, Könneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10(3):810-818. (Pubitemid 351160920)
19. Fuhrman JA, Davis AA (1997) Widespread Archaea and novel Bacteria from the deep sea as shown by 16S rRNA gene sequences. Mar Ecol Prog Ser 150:275-285.
20. López-García P, Moreira D, López-López A, Rodríguez-Valera F (2001) A novel hal-oarchaeal-related lineage is widely distributed in deep oceanic regions. Environ Microbiol 3(1):72-78.
21. Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409(6819):507-510. (Pubitemid 32144354)
22. DeLong EF, et al. (2006) Community genomics among stratified microbial assemblages in the ocean's interior. Science 311(5760):496-503. (Pubitemid 43157723)
23. Massana R, Murray AE, Preston CM, DeLong EF (1997) Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl Environ Microbiol 63(1):50-56.
24. Mincer TJ, et al. (2007) Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol 9(5):1162-1175. (Pubitemid 46697272)
25. Ottesen EA, et al. (2013) Pattern and synchrony of gene expression among sympatric marine microbial populations. Proc Natl Acad Sci USA 110(6):E488-E497.
26. Herfort L, et al. (2007) Variations in spatial and temporal distribution of Archaea in the North Sea in relation to environmental variables. FEMS Microbiol Ecol 62(3):242-257. (Pubitemid 350076064)
27. 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. (Pubitemid 38568199)
28. Galand PE, Casamayor EO, Kirchman DL, Potvin M, Lovejoy C (2009) Unique archaeal assemblages in the Arctic Ocean unveiled by massively parallel tag sequencing. ISME J 3(7):860-869.
29. Murray AE, et al. (1998) Seasonal and spatial variability of bacterial and archaeal assemblages in the coastal waters near Anvers Island, Antarctica. Appl Environ Microbiol 64(7):2585-2595. (Pubitemid 28303304)
30. López-García P, López-López A, Moreira D, Rodríguez-Valera F (2001) Diversity of free-living prokaryotes from a deep-sea site at the Antarctic Polar Front. FEMS Microbiol Ecol 36(2-3):193-202.
31. Alonso-Sáez L, Andersson A, Heinrich F, Bertilsson S (2011) High archaeal diversity in Antarctic circumpolar deep waters. Environ Microbiol Rep 3(6):689-697.
32. Hugoni M, 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(15):6004-6009.
33. Belmar L, Molina V, Ulloa O (2011) Abundance and phylogenetic identity of archaeoplankton in the permanent oxygen minimum zone of the eastern tropical South Pacific. FEMS Microbiol Ecol 78(2):314-326.
34. Michotey V, et al. (2012) Spatio-temporal diversity of free-living and particle-attached prokaryotes in the tropical lagoon of Ahe atoll (Tuamotu Archipelago) and its surrounding oceanic waters. Mar Pollut Bull 65(10-12):525-537.
35. Herndl GJ, et al. (2005) Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl Environ Microbiol 71(5):2303-2309. (Pubitemid 40646970)
36. Liu M, Xiao T, Wu Y, Zhou F, Zhang W (2011) Temporal distribution of the archaeal community in the Changjiang Estuary hypoxia area and the adjacent East China Sea as determined by denaturing gradient gel electrophoresis and multivariate analysis. Can J Microbiol 57(6):504-513.
37. DeLong EF (2006) Archaeal mysteries of the deep revealed. Proc Natl Acad Sci USA 103(17):6417-6418.
38. Turich C, et al. (2007) Lipids of marine Archaea: Patterns and provenance in the water-column and sediments. Geochim Cosmochim Acta 71(13):3272-3291. (Pubitemid 46908340)
39. Schouten S, van der Meer MTJ, Hopmans EC, Damsté JSS (2008) Comment on "Lipids of marine Archaea: Patterns and provenance in the water column and sediments" by Turich et al. (2007). Geochim Cosmochim Acta 72(21):5342-5346.
40. Turich C, et al. (2008) Reply to the Comment by S. Schouten, M. van der Meer, E. Hopmans, and J.S. Sinninghe Damsté on "Lipids of marine Archaea: Patterns and provenance in the water column.". Geochim Cosmochim Acta 72(21):5347-5349.
41. Caporaso JG, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335-336.
42. Frigaard N-U, Martínez A, Mincer TJ, DeLong EF (2006) Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439(7078):847-850. (Pubitemid 43255702)
43. Iverson V, et al. (2012) Untangling genomes from metagenomes: Revealing an uncultured class of marine Euryarchaeota. Science 335(6068):587-590.
44. DeLong EF, Taylor LT, Marsh TL, Preston CM (1999) Visualization and enumeration of marine planktonic archaea and bacteria by using polyribonucleotide probes and fluorescent in situ hybridization. Appl Environ Microbiol 65(12):5554-5563. (Pubitemid 129520650)
45. White DC, Davis WM, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40(1):51-62.
46. Liu X-L, Summons RE, Hinrichs K-U (2012) Extending the known range of glycerol ether lipids in the environment: Structural assignments based on tandem mass spectral fragmentation patterns. Rapid Commun Mass Spectrom 26(19):2295-2302.
47. Hopmans EC, Schouten S, Pancost RD, van der Meer MT, Sinninghe Damsté JS (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. (Pubitemid 30170360)
48. Ingalls A, Huguet C (2012) Distribution of intact and core membrane lipids of archaeal glycerol dialkyl glycerol tetraethers among size-fractionated particulate organic matter in Hood Canal, Puget Sound. Appl Environ Microbiol 78(5):1480-1490.
49. Lipp JS, Hinrichs K-U (2009) Structural diversity and fate of intact polar lipids in marine sediments. Geochim Cosmochim Acta 73(22):6816-6833.
50. Sturt HF, Summons RE, Smith K, Elvert M, Hinrichs K-U (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):617-628. (Pubitemid 38428873)
51. Wörmer L, Lipp JS, Schröder JM, Hinrichs K-U (2013) Application of two new LC-ESI-MS methods for improved detection of intact polar lipids (IPLs) in environmental samples. Org Geochem 59:10-21.
52. Jones DR, Karl DM, Laws EA (1996) Growth rates and production of heterotrophic bacteria and phytoplankton in the North Pacific subtropical gyre. Deep-Sea Research I 43(10):1567-1580.
53. Biddle JF, et al. (2006) Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci USA 103(10):3846-3851. (Pubitemid 43376643)
54. Lipp JS, Morono Y, Inagaki F, Hinrichs K-U (2008) Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 454(7207):991-994.
55. Schubotz F, Wakeham SG, Lipp JS, Fredricks HF, Hinrichs K-U (2009) Detection of microbial biomass by intact polar membrane lipid analysis in the water column and surface sediments of the Black Sea. Environ Microbiol 11(10):2720-2734.
56. Langworthy TA, Smith PF, Mayberry WR (1972) Lipids of Thermoplasma acidophilum. J Bacteriol 112(3):1193-1200.
57. Pearson A, et al. (2004) Nonmarine crenarchaeol in Nevada hot springs. Appl Environ Microbiol 70(9):5229-5237. (Pubitemid 39279594)
58. Pitcher A, Schouten S, Sinninghe Damsté JS (2009) In situ production of crenarchaeol in two California hot springs. Appl Environ Microbiol 75(13):4443-4451.
59. Pitcher A, et al. (2010) Crenarchaeol dominates the membrane lipids of Candidatus Nitrososphaera gargensis, a thermophilic group I.1b Archaeon. ISME J 4(4):542-552.
60. 86 paleothermometry. Paleoceanography 20(3):PA3013, 10.1029/2004PA001110.
61. 86 paleothermometry. Paleoceanography 21(4):PA4208, 10.1029/2006PA001279.
62. 86 paleothermometer in the ocean. Geochim Cosmochim Acta 72(4):1154-1173.
63. Pearson A, Ingalls AE (2013) Assessing the use of archaeal lipids as marine environmental proxies. Annu Rev Earth Planet Sci 41:359-384.
64. Pernthaler A, Preston CM, Pernthaler J, DeLong EF, Amann R (2002) Comparison of fluorescently labeled oligonucleotide and polynucleotide probes for the detection of pelagic marine bacteria and archaea. Appl Environ Microbiol 68(2):661-667. (Pubitemid 34113054)
65. Macalady JL, et al. (2004) Tetraether-linked membrane monolayers in Ferroplasma spp: A key to survival in acid. Extremophiles 8(5):411-419. (Pubitemid 39520729)
66. Schoon PL, et al. (2013) Recognition of Early Eocene global carbon isotope excursions using lipids of marine Thaumarchaeota. Earth Planet Sci Lett 373:160-168.
67. Wuchter C, et al. (2006) Archaeal nitrification in the ocean. Proc Natl Acad Sci USA 103(33):12317-12322. (Pubitemid 44267257)
68. Popendorf K, Lomas MW, Van Mooy BAS (2011) Microbial sources of intact polar diacylglycerolipids in the western North Atlantic Ocean. Org Geochem 42(7):803-811.
69. Teske A, Sørensen KB (2008) Uncultured archaea in deep marine subsurface sediments: Have we caught them all? ISME J 2(1):3-18. (Pubitemid 351612350)
70. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12:38.
71. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460-2461.
72. Ludwig W, et al. (2004) ARB: A software environment for sequence data. Nucleic Acids Res 32(4):1363-1371. (Pubitemid 38854737)
73. Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): An online tool for phylogenetic tree display and annotation. Bioinformatics 23(1):127-128. (Pubitemid 46017867)
74. Frias-Lopez J, et al. (2008) Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci USA 105(10):3805-3810. (Pubitemid 351723480)
75. Martínez A, Tyson GW, Delong EF (2010) Widespread known and novel phosphonate utilization pathways in marine bacteria revealed by functional screening and metagenomic analyses. Environ Microbiol 12(1):222-238.
76. Lohse M, et al. (2012) RobiNA: A user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res 40(Web Server issue):W622-7.
77. Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD (2012) PANDAseq: Paired-end assembler for illumina sequences. BMC Bioinformatics 13:31.
78. Kopylova E, Noé L, Touzet H (2012) SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28(24):3211-3217.
79. Kiełbasa SM, Wan R, Sato K, Horton P, Frith MC (2011) Adaptive seeds tame genomic sequence comparison. Genome Res 21(3):487-493.
80. Szymanski M, Barciszewska MZ, Barciszewski J, Erdmann VA (1999) 5S Ribosomal RNA data bank. Nucleic Acids Res 27(1):158-160. (Pubitemid 29209424)
81. Huson DH, Mitra S, Ruscheweyh HJ, Weber N, Schuster SC (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res 21(9):1552-1560.
82. Huguet C, et al. (2006) An improved method to determine the absolute abundance of glycerol dibiphytanyl glycerol tetraether lipids. Org Geochem 37(9):1036-1041. (Pubitemid 44292844)