Abundance and phylogenetic identity of archaeoplankton in the permanent oxygen minimum zone of the eastern tropical South Pacific

FEMS Microbiology Ecology

Volumn 78, Issue 2, 2011, Pages 314-326

  Belmar, Lucy ^a   Molina, Verónica ^a   Ulloa, Osvaldo ^a  

^a UNIVERSITY OF CONCEPCIÓN   (Chile)

Author keywords

Crenarchaea; Euryarchaea; Suboxic

Indexed keywords

OXYGEN; SEA WATER;

COMMUNITY STRUCTURE; DEEP SEA; HYBRIDIZATION; HYDROTHERMAL VENT; PHYLOGENETICS; PHYLOGENY; PROKARYOTE; RELATIVE ABUNDANCE; SPECIES DIVERSITY; SPECIES RICHNESS; SUBOXIC CONDITIONS;

ARCHAEBACTERIUM; ARTICLE; CHEMISTRY; CLASSIFICATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYDROTHERMAL VENT; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANKTON; RNA GENE; TROPIC CLIMATE;

ARCHAEA; GENES, RRNA; HYDROTHERMAL VENTS; MOLECULAR SEQUENCE DATA; OXYGEN; PHYLOGENY; PLANKTON; SEAWATER; TROPICAL CLIMATE;

PACIFIC OCEAN; PACIFIC OCEAN (SOUTH);

ARCHAEA; CANDIDATUS NITROSOPUMILUS MARITIMUS; CRENARCHAEOTA; EURYARCHAEOTA; MARINE GROUP II;

EID: 80054098909     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2011.01159.x     Document Type: Article

References (76)

1. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ & Weightman AJ (2005) At least 1 in 20 16S rRNA sequence records currently held in repositories is estimated to contain substantial anomalies. Appl Environ Microb71: 7724-7736.
2. Auguet JC & Casamayor EO (2008) A hotspot for cold Crenarchaeota in the neuston of high mountain lakes. Environ Microbiol10: 1080-1086.
3. Beman JM, Popp BN & Francis CA (2008) Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J2: 429-441.
4. Beman JM, Sachdeva R & Fuhrman JA (2010) Population ecology of nitrifying Archaea and Bacteria in the Southern California Bight. Environ Microbiol12: 1282-1292.
5. Blanco JL, Thomas AL, Carr ME & Strub PT (2001) Seasonal climatology of hydrographic conditions in the upwelling region off northern Chile. J Geophys Res106: 11451-11467.
6. Brochier-Armanet C, Boussau B, Gribaldo S & Forterre F (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum the Thaumarchaeota. Nat Rev Microbiol 6: 245-252.
7. Canfield DE, Stewart FJ, Thamdrup B, De Brabandere L, Dalsgaard T, Delong EF, Revsbech NP & Ulloa O (2010) A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast. Science330: 1375-1378.
8. Castro-González M, Braker G, Farías L & Ulloa O (2005) Communities of nirS-type denitrifiers in the water column of the oxygen minimum zone in the eastern South Pacific. Environ Microbiol9: 1298-1306.
9. Church MJ, Wai B, Karl DM & DeLong EF (2010) Abundances of crenarchaeal amoA genes and transcripts in the Pacific Ocean. Environ Microbiol12: 679-688.
10. Codispoti LA, Friederich GE, Packard TTet al. (1986) High nitrite levels off Northern Peru: a signal of instability in the marine denitrification rate. Science 233: 1200-1202.
11. Coolen MJL, Abbas B, van Bleijswijk J, Hopmans EC, Kuypers MMM, Wakeham SG & Sinninghe Damsté JS (2007) Putative ammonia-oxidizing Crenarchaeota in suboxic waters of the Black Sea: a basin-wide ecological study using 16S ribosomal and functional genes and membrane lipids. Environ Microbiol 9: 1001-1016.
12. DeLong EF (1992) Archaea in coastal marine environments. P Natl Acad Sci USA89: 5685-5689.
13. DeLong EF (1998) Everything in moderation: archaea as 'non-extremophiles'. Curr Opin Genet Dev 8: 649-654.
14. 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 Microb65: 5554-5563.
15. Farías L, Paulmier A & Gallegos M (2007) Nitrous oxide and N-nutrient cycling in the oxygen minimum zone off northern Chile. Deep-Sea Res Pt I54: 164-180.
16. Farías L, Castro-González M, Cornejo M, Charpentier J, Faúndez J, Boontanon N & Yoshida N (2009) Denitrification and nitrous oxide cycling within the upper oxycline of the eastern tropical South Pacific oxygen minimum zone. Limnol Oceanogr54: 132-144.
17. Feinstein LM, Sul WJ & Blackwood CB (2009) Assessment of bias associated with incomplete extraction of microbial DNA from soil. Appl Environ Microb75: 5428-5433.
18. 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. P Natl Acad Sci USA102: 14683-14688.
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 Ser150: 275-285.
20. Galán A, Molina V, Thamdrup B, Woebken D, Lavik G, Kuypers MM & Ulloa O (2009) Anammox bacteria and the anaerobic oxidation of ammonium in the oxygen minimum zone off northern Chile. Deep-Sea Res Pt II56: 1021-1031.
21. Guindon S & Gascuel O (2003) A simple fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol52: 696-704.
22. Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe Y-I, Sugahara J, Preston C, de la Torre J, Richardson PM & DeLong EF (2006a) Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. P Natl Acad Sci USA103: 18296-18301.
23. Hallam SJ, Mincer TJ, Schleper C, Preston CM, Roberts K, Richardson P & DeLong EF (2006b) Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol4: e95.
24. Hamersley MR, Lavik G, Woebken Det al. (2007) Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone. Limnol Oceanogr52: 923-933.
25. Helly J & Levin L (2004) Global distribution of naturally occurring marine hypoxia on continental margins. Deep-Sea Res Pt I51: 1159-1168.
26. Herfort L, Schouten S, Abbas B, Veldhuis MJW, Coolen MJL, Wuchter C, Boon JP, Herndl GJ & Sinninghe Damsté JS (2007) Variations in spatial and temporal distribution of Archaea in the North Sea in relation to environmental variables. FEMS Microbiol Ecol62: 242-257.
27. Hershberger KL, Barns SM, Reysenbach AL, Dawson SC & Pace NR (1996) Wide diversity of Crenarchaeota. Nature384: 420.
28. Holmes RM, Aminot A, Kerouel R, Hooker BA & Peterson BJ (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci56: 1801-1808.
29. Huber T, Faulkner G & Hugenholtz P (2004) Bellerophon; a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics20: 2317-2319.
30. Jurgens G, Lindström K & Saano A (1997) Novel group within the kingdom Crenarchaeota from boreal forest soil. Appl Environ Microb63: 803-805.
31. Kamykowski DZ & Zentara SJ (1990) Hypoxia in the world ocean as recorded in the historical data set. Deep-Sea Res37: 1861-1874.
32. Karner MB, DeLong EF & Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature409: 507-510.
33. Katoh K, Misawa K, Kuma K & Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066.
34. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB & Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature437: 543-546.
35. Lam P, Jensen M, Lavik G, McGinnis D, Müller B, Schubert C, Amann R, Thamdrup B & Kuypers M (2007) Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. P Natl Acad Sci USA104: 7104-7109.
36. Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D, Gutiérrez D, Amann R, Jetten MSM & Kuypers MMM (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. P Natl Acad Sci USA106: 4752-4757.
37. Lin X, Wakeham S, Putnam I, Astor Y, Scranton M, Chistoserdov A & Taylor G (2006) Comparison of vertical distributions of prokaryotic assemblages in the anoxic Cariaco Basin and Black Sea by use of fluorescence in situ hybridization. Appl Environ Microb72: 2679-2690.
38. Llirós M, Gich F, Plasencia A, Auguet J-C, Darchambeau F, Casamayor EO, Descy J-P & Borrego C (2010) Vertical distribution of ammonia-oxidizing Crenarchaeota and methanogens in the epipelagic waters of Lake Kivu (Rwanda-Democratic Republic of the Congo). Appl Environ Microb76: 6853-6863.
39. López-García P, Moreira D, López-López A & Rodríguez-Valera F (2001) A novel haloarchaeal-related lineage is widely distributed in deep oceanic regions. Environ Microbiol3: 72-78.
40. Madrid V, Taylor G & Scranton M (2001) Phylogenetic diversity of bacterial and archaeal communities in the anoxic zone of the Cariaco Basin. Appl Environ Microb67: 1663-1674.
41. Marie D, Partensky F, Jacquet S & Vaulot D (1997) Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl Environ Microb63: 186-193.
42. Martin-Cuadrado AB, Rodríguez-Valera F, Moreira D, Alba JC, Ivars-Martínez E, Henn MR, Talla E & López-García P (2008) Hindsight in the relative abundance metabolic potential and genome dynamics of uncultivated marine archaea from comparative metagenomic analyses of bathypelagic plankton of different oceanic regions. ISME J2: 865-886.
43. 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 Microb63: 50-56.
44. Massana R, Taylor LT, Murray AE, Wu KY, Jeffrey WH & DeLong EF (1998) Distribution of marine planktonic archaea in the Gerlache strait Antarctic Peninsula during early spring. Limnol Oceanogr43: 607-617.
45. Massana R, DeLong EF & Pedrós-Alió C (2000) A few cosmopolitan phylotypes dominate planktonic archaeal assemblages in widely different oceanic provinces. Appl Environ Microb66: 1777-1787.
46. Mincer TJ, Church MJ, Taylor LT, Preston C, Karl DM & DeLong EF (2007) Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol9: 1162-1175.
47. Molina V & Farías L (2009) Aerobic ammonium oxidation in the oxycline and oxygen minimum zone of the eastern tropical South Pacific off northern Chile (20°S). Deep-Sea Res Pt II56: 1032-1041.
48. Molina V, Farías L, Eissler Y, Cuevas LA, Morales CE & Escribano R (2005) Ammonium cycling under a strong oxygen gradient associated with the Oxygen Minimum Zone off northern Chile (∼23°S). Mar Ecol-Prog Ser288: 35-43.
49. Molina V, Belmar L & Ulloa O (2010) High diversity of ammonia-oxidizing archaea in permanent and seasonal oxygen-deficient waters of the eastern South Pacific. Environ Microbiol12: 2450-2465.
50. Morgan JL, Darling AE & Eisen JA (2010) Metagenomic sequencing of an in vitro-simulated microbial community. PLoS One5: e10209.
51. Murray A, Blakis A, Massana R, Strawzewski S, Passow U, Alldredge A & DeLong E (1999) A time series assessment of planktonic archaeal variability in the Santa Barbara Channel. Aquat Microb Ecol20: 129-145.
52. Park B-J, Park S-J, Yoon D-N, Schouten S, Sinninghe Damsté JS & Rhee S-K (2010) Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in co-culture with sulphur-oxidizing bacteria. Appl Environ Microb76: 7575-7587.
53. Posada D (2008) JModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
54. Quiñones RA, Levipan HA & Urrutia H (2009) Spatial and temporal variability of planktonic archaeal abundance in the Humboldt Current System off Chile. Deep-Sea Res Pt II56: 1073-1082.
55. Ramírez-Flandes S & Ulloa O (2008) Bosque: integrated phylogenetic analysis software. Bioinformatics 24: 2539-2541.
56. Revsbech NP, Larsen LH, Gundersen J, Dalsgaard T, Ulloa O & Thamdrup B (2009) Determination of ultra-low oxygen concentrations in oxygen minimum zones by the STOX sensor. Limnol Oceanogr-Meth7: 371-381.
57. Santoro AE, Casciotti KL & Francis CA (2010) Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current. Environ Microbiol12: 1989-2006.
58. Schneider W, Fuenzalida R, Rodríguez-Rubio E, Garcés-Vargas J & Bravo L (2003) Characteristics and formation of Eastern South Pacific intermediate water. Geophys Res Lett30: 1-4.
59. Sinninghe Damsté JS, Rijpstra WIC, Hopmans EC, Prahl FG, Wakeham SG & Schouten S (2002) Distribution of membrane lipids of planktonic Crenarchaeota in the Arabian Sea. Appl Environ Microb68: 2997-3002.
60. Stevens H & Ulloa O (2008) Bacterial diversity in the oxygen minimum zone of the eastern tropical South Pacific. Environ Microbiol10: 1244-1259.
61. Stewart FJ, Ulloa O & DeLong EF (2011) Microbial metatranscriptomics in a permanent marine oxygen minimum zone. Environ Microbiol. DOI: DOI: 10.1111/j.1462-2920.2010.02400.x.
62. Sunamura M, Higashi Y, Miyako C, Ishibashi J-I & Maruyama A (2004) Two bacteria phylotypes are predominant in the Suiyo Seamount hydrothermal plume. Appl Environ Microb70: 1190-1198.
63. Takai K & Horikoshi K (1999) Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics152: 1285-1297.
64. Talavera G & Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol56: 564-577.
65. Teira E, Reinthaler T, Pernthaler A, Pernthaler J & Herdl GJ (2004) Combining catalyzed reporter deposition fluorescence in situ hybridization and microautoradiography to detect substrate utilization by Bacteria and Archaea in the deep ocean. Appl Environ Microb70: 4411-4414.
66. Teske A & Sørensen KB (2008) Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME J 2: 3-18.
67. Thamdrup B, Jensen MM, Dalsgaard T, Ulloa O, Farías L & Escribano R (2006) Anaerobic ammonium oxidation in the oxygen-deficient water off northern Chile. Limnol Oceanogr51: 2145-2156.
68. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk H & Schleper S (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol7: 1985-1995.
69. Venter JC, Remington K, Heidelberg JFet al. (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science304: 66-74.
70. 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 Microb65: 4375-4384.
71. Vetriani C, Tran H & Kerkhof L (2003) Fingerprinting microbial assemblages from the oxic/anoxic chemocline of the Black Sea. Appl Environ Microb69: 6481-6488.
72. Walker CB, de la Torre JR, Klotz MGet al. (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. P Natl Acad Sci USA107: 8818-8823.
73. Wallner G, Amann R & Beisker W (1993) Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry14: 136-143.
74. Whitmire AL, Letelier RM, Villagrán V & Ulloa O (2009) Autonomous observations of in vivo fluorescence and particle backscattering in an oceanic oxygen minimum zone. Opt Express17: 21992-22004.
75. Woebken D, Fuchs B, Kuypers MM & Amann R (2007) Potential interactions of particle-associated anammox bacteria with bacterial and archaeal partners in the Namibian upwelling system. Appl Environ Microb73: 4648-4657.
76. Wuchter C, Abbas B, Coolen MJLet al. (2006) Archaeal nitrification in the ocean. P Natl Acad Sci USA103: 12317-12322.