377
Views
3
CrossRef citations to date
0
Altmetric
Original Articles

Aerobic and Anaerobic Ammonia-Oxidizing Microorganisms in Low-Temperature Hydrothermal Fe-Si-rich Precipitates of the Southwestern Pacific Ocean

, , , , , , & show all
Pages 42-52 | Received 01 Feb 2013, Accepted 01 Apr 2013, Published online: 25 Oct 2013

References

  • Alt , JC. 1988 . Hydrothermal oxide and nontronite deposits on seamounts in the Eastern Pacific . Mar Geol , 81 : 227 – 239 .
  • Avrahami , S and Conrad , R . 2003 . Patterns of community change among ammonia oxidizers in meadow soils upon long-term incubation at different temperatures . Appl Environ Microbiol , 69 : 6152 – 6164 .
  • Bemis , K , Lowell , R P and Farough , A . 2012 . Diffuse flow on and around hydrothermal vents at mid-ocean ridges . Oceanogr , 25 : 182 – 191 .
  • Bourbonnais , A , Lehmann , M F , Butterfield , D A and Juniper , S K . 2012 . Subseafloor nitrogen transformations in diffuse hydrothermal vent fluids of the Juan de Fuca Ridge evidenced by the isotopic composition of nitrate and ammonium . Geochem Geophys Geosyst , 13 : Q02T01 doi: 10.1029/2011GC003863
  • Boyd , T D and Scott , S D . 2001 . Microbial and hydrothermal aspects of ferric oxyhydroxides and ferrosic hydroxides: the example of Franklin Seamount, Western Woodlark Basin, Papua New Guinea . Geochem Trans , 2 : 45
  • Brochier-Armanet , C , Boussau , B , Gribaldo , S and Forterre , P . 2008 . Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota . Nat Rev Microbiol , 6 : 245 – 252 .
  • Campbell , M A , Chain , P SG , Dang , H , El Sheikh , A F , Norton , J M , Ward , N L , Ward , B B and Klotz , M G . 2011 . Nitrosococcus watsonii sp. nov., a new species of marine obligate ammonia-oxidizing bacteria that is not omnipresent in the world's oceans: calls to validate the names Nitrosococcus halophilus and Nitrosomonas mobilis . FEMS Microbiol Ecol , 76 : 39 – 48 .
  • Cao , H , Hong , Y , Li , M and Gu , J D . 2012 . Community shift of ammonia-oxidizing bacteria along an anthropogenic pollution gradient from the Pearl River Delta to the South China Sea . Appl Microbiol Biotechnol , 94 : 247 – 259 .
  • Chain , P , Lamerdin , J , Larimer , F , Regala , W , Lao , V , Land , M , Hauser , L , Hooper , A , Klotz , M , Norton , J , Sayavedra-Soto , L , Arciero , D , Hommes , N , Whittaker , M and Arp , D . 2003 . Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea . J Bacteriol , 185 : 2759 – 2773 .
  • Christman , G D , Cottrell , M T , Popp , B N , Gier , E and Kirchman , D L . 2011 . Abundance, diversity, and activity of ammonia-oxidizing prokaryotes in the coastal Arctic Ocean in summer and winter . Appl Environ Microbiol , 77 : 2026 – 2034 .
  • Corliss , J B , Dymond , J , Gordon , L I , Edmond , J M , Von Herzen , R P , Ballard , R D , Green , K , Williams , D , Bainbridge , A , Crane , K and Van Andel , T H . 1979 . Submarine thermal springs on the Galapagos Rift . Science , 203 : 1073 – 1083 .
  • Dalsgaard , T , Thamdrup , B and Canfield , D E . 2005 . Anaerobic ammonium oxidation (anammox) in the marine environment . Res Microbiol , 156 : 457 – 464 .
  • Dang , H , Li , J , Chen , R , Wang , L , Luo , L , Zhang , Z and Klotz , M G . 2010 . Diversity, abundance and spatial distribution of sediment ammonia-oxidizing Betaproteobacteria in response to environmental gradients and coastal eutrophication in Jiaozhou Bay, China . Appl Microbiol Ecol , 76 : 4691 – 4702 .
  • Dang , H , Li , J , Zhang , X , Li , T , Tian , F and Jin , W . 2009 . Diversity and spatial distribution of amoA-encoding archaea in the deep-sea sediments of the tropical West Pacific Continental Margin . J Appl Microbiol , 106 : 1482 – 1493 .
  • Davis , R E , Stakes , D S , Wheat , C G and Moyer , C L . 2009 . Bacterial variability within an Fe-Si-Mn-rich hydrothermal mound located off-axis at the Cleft Segment, Juan de Fuca Ridge . Geomicrobiol J , 26 : 570 – 580 .
  • De Corte , D , Yokokawa , T , Varela , M M , Agogue , H and Herndl , G J . 2009 . Spatial distribution of Bacteria and Archaea and amoA gene copy numbers throughout the water column of the Eastern Mediterranean Sea . ISME J , 3 : 147 – 158 .
  • Dekov , V M , Petersen , S , Garbe-Schonberg , C D , Kamenov , G D , Perner , M , Kuzmann , E and Schmidt , M . 2010 . Fe-Si-oxyhydroxide deposits at a slow-spreading centre with thickened oceanic crust: The Lilliput hydrothermal field (9°33′S, Mid-Atlantic Ridge) . Chem Geol , 278 : 186 – 200 .
  • DeSantis , T Z , Hugenholtz , P , Keller , K , Brodie , E L , Larsen , N , Piceno , Y M , Phan , R and Andersen , G L . 2006 . NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes . Nucleic Acids Res , 34 : W394 – 399 .
  • Edwards , K J , Glazer , B T , Rouxel , O J , Bach , W , Emerson , D , Davis , R E , Toner , B M , Chan , C S , Tebo , B M , Staudigel , H and Moyer , C L . 2011 . Ultra-diffuse hydrothermal venting supports Fe-oxidizing bacteria and massive number deposition at 5000m off Hawaii . ISME J , 5 : 1748 – 1758 .
  • Emerson , D and Moyer , C L . 1997 . Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH . Appl Environ Microbiol , 63 : 4784 – 4792 .
  • Emerson , D and Moyer , C L . 2002 . Neutrophilic Fe-oxidizing bacteria are abundant at the Loihi Seamount hydrothermal vents and play a major role in Fe oxide deposition . Appl Environ Microbiol , 68 : 3085 – 3093 .
  • Fernandez-Guerra , A and Casamayor , E O . 2012 . Habitat-Associated Phylogenetic Community Patterns of Microbial Ammonia Oxidizers . PLoS ONE , 7 : e47330
  • Forget , N L , Murdock , S A and Juniper , S K . 2010 . Bacterial diversity in Fe-rich hydrothermal sediments at two South Tonga Arc submarine volcanoes . Geobiology , 8 : 417 – 432 .
  • Francis , C A , Beman , J M and Kuypers , M MM . 2007 . New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation . ISME J , 1 : 19 – 27 .
  • Francis , C A , O’Mullan , G D and Ward , B B . 2003 . Diversity of ammonia monooxygenase (amoA) genes across environmental gradients in Chesapeake Bay sediments . Geobiology , 1 : 129 – 140 .
  • Francis , C A , Roberts , K J , Beman , J M , Santoro , A E and Oakley , B B . 2005 . Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean . Proc Natl Acad Sci USA , 102 : 14683 – 14688 .
  • Galán , A , Molina , V , Thamdrup , B , Woebken , D , Lavik , G , Kuypers , M MM and Ulloa , O . 2009 . Anammox bacteria and the anaerobic oxidation of ammonium in the oxygen minimum zone off northern Chile . Deep-Sea Res II , 56 : 1021 – 1031 .
  • Harhangi , H R , Le Roy , M , van Alen , T , Hu , B L , Groen , J , Kartal , B , Tringe , S G , Quan , Z X , Jetten , M S and Op den Camp , H J . 2012 . Hydrazine synthase, a unique phylomarker with which to study the presence and biodiversity of anammox bacteria . Appl Environ Microbiol , 78 : 752 – 758 .
  • Hayashi , T , Kaneko , R , Tanahashi , M and Naganuma , T . 2007 . Molecular diversity of the genes encoding ammonia monooxygenase and particulate methane monooxygenase from deep-sea sediments . Res J Microbiol , 2 : 530 – 537 .
  • Hopmans , E C , Weijers , J WH , Schefuss , E , Herfort , L , Sinninghe Damsté , J S and Schouten , S . 2004 . A novel proxy for terrestrial organic matter in sediments based on branched and isoprenoid tetraether lipids . Earth Planet Sci Lett , 224 : 107 – 116 .
  • Huber , T , Faulkner , G and Hugenholtz , P . 2004 . Bellerophon: a program to detect chimeric sequences in multiple sequence alignments . Bioinformaticsatics , 20 : 2317 – 2319 .
  • Huguet , C , Hopmans , E C , Febo-Ayala , W , Thompson , D H , Sinninghe Damsté , J S and Schouten , S . 2006 . An improved method to determine the absolute abundance of glycerol dibiphytanyl glycerol tetraether lipids . Org Geochem , 37 : 1036 – 1041 .
  • Jetten , M S , Niftrik , L , Strous , M , Kartal , B , Keltjens , J T and Op den Camp , H J . 2009 . Biochemistry and molecular biology of anammox bacteria . Crit Rev Biochem Mol Biol , 44 : 65 – 84 .
  • Juniper , S K and Fouquet , Y . 1988 . Filamentous iron-silica deposits from modern and ancient hydrothermal sites . Can Mineral , 26 : 859 – 869 .
  • Kato , S , Kobayashi , C , Kakegawa , T and Yamagishi , A . 2009 . Microbial communities in iron-silica-rich microbial mats at deep-sea hydrothermal fields of the southern Mariana Trough . Environ Microbiol , 11 : 2094 – 2111 .
  • Kato , S , Nakamura , K , Toki , T , Ishibashi , J-i , Tsunogai , U , Hirota , A , Ohkuma , M and Yamagishi , A . 2012 . Iron-based microbial ecosystem on and below the seafloor: a case study of hydrothermal fields of the Southern Mariana Trough . Front Microbiol , 3 : 89
  • Kim , O S , Junier , P , Imhoff , J F and Witzel , K P . 2008 . Comparative analysis of ammonia monooxygenase (amoA) genes in the water column and sediment-water interface of two lakes and the Baltic Sea . FEMS Microbiol Ecol , 66 : 367 – 378 .
  • Konneke , M , Bernhard , A E , de la Torre , J R , Walker , C B , Waterbury , J B and Stahl , D A . 2005 . Isolation of an autotrophic ammonia-oxidizing marine archaeon . Nature , 437 : 543 – 546 .
  • Kowalchuk , G A and Stephen , J R . 2001 . Ammonia-oxidizing bacteria: a model for molecular microbial ecology . Annu Rev Microbiol , 55 : 485 – 529 .
  • Kuypers , M M , Sliekers , A O , Lavik , G , Schmid , M , Jørgensen , B B , Kuenen , J G , Sinninghe Damsté , J S , Strous , M and Jetten , M S . 2003 . Anaerobic ammonium oxidation by anammox bacteria in the Black Sea . Nature , 422 : 608 – 611 .
  • Lam , P , Lavik , G , Jensen , M M , van de Vossenberg , J , Schmid , M , Woebken , D , Gutiérrezc , D , Amanna , R , Mike , S. M. , Jettenb , M SM and Kuypersa , M MM . 2009 . Revising the nitrogen cycle in the Peruvian oxygen minimum zone . Proc Natl Natl Acad Sci USA , 106 : 4752 – 4757 .
  • Larkin , M A , Blackshields , G , Brown , N P , Chenna , R , McGettigan , P A , McWilliam , H , Valentin , F , Wallace , I M , Wilm , A , Lopez , R , Thompson , J D , Gibson , T J and Higgins , D G . 2007 . Clustal W and Clustal X version 2.0 . Bioinformatics , 23 : 2947 – 2948 .
  • Lee , Z M , Bussema , C and Schmidt , T M . 2009 . rrnDB: documenting the number of rRNA and tRNA genes in bacteria and archaea . Nucl Acids Res , 37 : D489 – D493 .
  • Lengger , S , Hopmans , E C , Sinninghe Damsté , J S and Schouten , S . 2012 . Comparison of extraction and work up techniques for analysis of core and intact polar tetraether lipids from sedimentary environments . Org Geochem , 47 : 34 – 40 .
  • Li , J , Zhou , H , Peng , X , Wu , Z , Chen , S and Fang , J . 2012 . Microbial diversity and biomineralization in low-temperature hydrothermal iron–silica-rich precipitates of the Lau Basin hydrothermal field . FEMS Microbiol Ecol , 81 : 205 – 216 .
  • McAllister , S M , Davis , R E , McBeth , J M , Tebo , B M , Emerson , D and Moyer , C L . 2011 . Biodiversity and emerging biogeography of the neutrophilic iron-oxidizing zetaproteobacteria . Appl Environ Microbiol , 77 : 5445 – 5457 .
  • Mincer , T J , Church , M J , Taylor , L T , Preston , C , Karl , D M and DeLong , E F . 2007 . Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre . Environ Microbiol , 9 : 1162 – 1175 .
  • Mulder , A , Graaf , A A , Robertson , L A and Kuenen , J G . 1995 . Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor . FEMS Microbiol Ecol , 16 : 177 – 184 .
  • Nakagawa , T , Mori , K , Kato , C , Takahashi , R and Tokuyama , T . 2007 . Distribution of cold-adapted ammonia-oxidizing microorganisms in the deep-ocean of the northeastern Japan Sea . Microbes Environ , 22 : 365 – 372 .
  • Nold , S C , Zhou , J , Devol , A H and Tiedje , J M . 2000 . Pacific Northwest marine sediments contain ammonia-oxidizing bacteria in the beta subdivision of the Proteobacteria . Appl Environ Microbiol , 66 : 4532 – 4535 .
  • Nunoura , T , Oida , H , Nakaseama , M , Kosaka , A , Ohkubo , S B , Kikuchi , T , Kazama , H , Hosoi-Tanabe , S , Nakamura , K , Kinoshita , M , Hirayama , H , Inagaki , F , Tsunogai , U , Ishibashi , J and Takai , K . 2010 . Archaeal diversity and distribution along thermal and geochemical gradients in hydrothermal sediments at the Yonaguni Knoll IV hydrothermal field in the Southern Okinawa Trough . Appl Environ Microbiol , 76 : 1198 – 1211 .
  • O’Mullan , G D and Ward , B B . 2005 . Relationship of temporal and spatial variabilities of ammonia-oxidizing bacteria to nitrification rates in Monterey Bay, California . Appl Environ Microbiol , 71 : 697 – 705 .
  • Orcutt , B N , Sylvan , J B , Knab , N J and Edwards , K J . 2011 . Microbial ecology of the dark ocean above, at, and below the seafloor . Microbiol Mol Biol Rev , 75 : 361 – 422 .
  • Pearson , A , Huang , Z , Ingalls , A E , Romanek , C S , Wiegel , J , Freeman , K H , Smittenberg , R H and Zhang , C L . 2004 . Nonmarine crenarchaeol in Nevada hot springs . Appl Environ Microbiol , 70 : 5229 – 5237 .
  • Peng , X , Chen , S , Zhou , H , Zhang , L , Li , J , Li , J and Wu , Z . 2011 . Diversity of biogenic minerals in low temperature Si-rich deposits from a newly discovered hydrothermal field on the ultra-slow spreading Southwest Indian Ridge . J Geophy Res , 116 : G03030
  • Penton , C R , Devol , A H and Tiedje , J M . 2006 . Molecular evidence for the broad distribution of anammox bacteria in freshwater and marine sediments . Appl Environ Microbiol , 72 : 6829 – 6832 .
  • Pester , M , Rattei , T , Flechl , S , Grongroft , A , Richter , A , Overmann , J , Reinhold-Hurek , B , Loy , A and Wagner , M . 2012 . amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions . Environ Microbiol , 14 : 525 – 539 .
  • Pitcher , A , Hopmans , E C , Mosier , A C , Park , S J , Rhee , S K , Francis , C A , Schouten , S and Damsté , J S . 2011 . Core and intact polar glycerol dibiphytanyl glycerol tetraether lipids of ammonia-oxidizing archaea enriched from marine and estuarine sediments . Appl Envir Microbiol , 77 : 3468 – 3477 .
  • Purkhold , U , Pommerening-Roser , A , Juretschko , S , Schmid , M C , Koops , H P and Wagner , M . 2000 . Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence aalysis: implications for molecular diversity surveys . Appl Environ Microbiol , 66 : 5368 – 5382 .
  • Rassa , A C , McAllister , S M , Safran , S A and Moyer , C L . 2009 . Zeta-proteobacteria dominate the colonization and formation of microbial mats in low-temperature hydrothermal vents at Loihi Seamount, Hawaii . Geomicrobiol J , 26 : 623 – 638 .
  • Rotthauwe , J H , Witzel , K P and Liesack , W . 1997 . The ammonia monooxygenase structural gene amoA as a functional marker: Molecular fine-scale analysis of natural ammonia oxidizing populations . Appl Environ Microbiol , 63 : 4704 – 4712 .
  • Roussel , E G , Sauvadet , A L , Chaduteau , C , Fouquet , Y , Charlou , J L , Prieur , D and Cambon Bonavita , M A . 2009 . Archaeal communities associated with shallow to deep subseafloor sediments of the New Caledonia Basin . Environ Microbiol , 11 : 2446 – 2462 .
  • Santoro , A E , Casciotti , K L and Francis , C A . 2010 . Activity, abundance and diversity of nitrifying arhaea and bacteria in the central California Current . Environ Microbiol , 12 : 1989 – 2006 .
  • Schloss , P D and Handelsman , J . 2005 . Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness . Appl Environ Microbiol , 71 : 1501 – 1506 .
  • Schmid , M , Walsh , K , Webb , R , Rijpstra , W IC , van de Pas-Schoonen , K , Verbruggen , M J , Hill , T , Moffett , B , Fuerst , J , Schouten , S , Damste , J SS , Harris , J , Shaw , P , Jetten , M and Strous , M . 2003 . Candidatus “Scalindua brodae”, sp. nov., Candidatus “Scalindua wagneri”, sp. nov., two new species of anaerobic ammonium oxidizing bacteria . Syst Appl Microbiol , 26 : 529 – 538 .
  • Schmid , M C , Risgaard-Petersen , N , van de Vossenberg , J , Kuypers , M MM , Lavik , G , Petersen , J , Hulth , S , Thamdrup , B , Canfield , D , Dalsgaard , T , Rysgaard , S , Sejr , M K , Strous , M , den Camp , H J and Jetten , M S . 2007 . Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity . Environ Microbiol , 9 : 1476 – 1484 .
  • Schouten , S , Hopmans , E C and Sinninghe Damsté , J S . 2013 . The organic geochemistry of glycerol dialkyl glycerol tetraether lipids: A review . Org Geochem , 54 : 19 – 61 .
  • Schouten , S , Huguet , C , Hopmans , E C , Kienhuis , M V and Damsté , J S . 2007 . Analytical methodology for TEX86 paleothermometry by high-performance liquid chromatography/atmospheric pressure chemical ionization- mass spectrometry . Anal Chem , 79 : 2940 – 2944 .
  • SRK Consulting Report for Nautilus Minerals . 2008 . 2008 Exploration Program Papua New Guinea, Tonga, Fiji, Solomon Islands and New Zealand, Nautilus Minerals Inc . West Perth, Australia: SRK Consulting. Available online at: http://www.nautilusminerals.com/i/pdf/2008NautilusExplorationNI43-101Report.pdf
  • Stahl , D A and de la Torre , J R . 2012 . Physiology and diversity of ammonia-oxidizing archaea . Annu Rev Microbiol , 66 : 83 – 101 .
  • Stephen , J R , McCaig , A E , Smith , Z , Prosser , J I and Embley , T M . 1996 . Molecular diversity of soil and marine 16S rDNA sequences related to b-subgroup ammonia oxidising bacteria . Appl Environ Microbiol , 62 : 4147 – 4154 .
  • Sturt , H F , Summons , R E , Smith , K , Elvert , M and Hinrichs , K U . 2004 . Intact polar membrane lipids in prokaryotes and sediments deciphered by highperformance liquid chromatography/electrospray ionization multistage mass spectrometry-new biomarkers for biogeochemistry and microbial ecology . Rapid Commun Mass Sp , 18 : 617 – 628 .
  • Tamura , K , Peterson , D , Peterson , N , Stecher , G , Nei , M and Kumar , S . 2011 . MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods . Mol Biol Evol , 28 : 2731 – 2739 .
  • Tivey , M K , Becker , E , Beinart , R , Fisher , C R , Girguis , P R , Langmuir , C H , Michael , P J and Reysenbach , A-L . 2012 . Links from mantle to microbe at the Lau Integrated Study Site: Insights from a back-arc spreading center . Oceanogr , 25 : 62 – 77 .
  • Urakawa , H , Tajima , Y , Numata , Y and Tsuneda , S . 2008 . Low temperature decreases the phylogenetic diversity of ammonia-oxidizing archaea and bacteria in aquarium biofiltration systems . Appl Environ Microbiol , 74 : 894 – 900 .
  • Wang , S , Xiao , X , Jiang , L , Peng , X , Zhou , H , Meng , J and Wang , F . 2009 . Diversity and abundance of ammonia-oxidizing archaea in hydrothermal vent chimneys of the Juan de Fuca Ridge . Appl Environ Microbiol , 75 : 4216 – 4220 .
  • Woebken , D , Fuchs , B M , Kuypers , M MM and Amann , R . 2007 . Potential interactions of particle-associated anammox bacteria with bacteria and archaeal partners in the Namibian upwelling system . Appl Environ Microbiol , 73 : 4648 – 4657 .
  • Woebken , D , Lam , P , Kuypers , M MM , Naqvi , S W , Kartal , B , Strous , M , Jetten , M S , Fuchs , B M and Amann , R . 2008 . A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones . Environ Microbiol , 10 : 3106 – 3119 .
  • Wuchter , C , Abbas , B , Coolen , M JL , Herfort , L , van Bleijswijk , J , Timmers , P , Strous , M , Teira , E , Herndl , G J , Middelburg , J J , Schouten , S and Sinninghe Damste , J S . 2006 . Archaeal nitrification in the ocean . Proc Natl Acad Sci USA , 103 : 12317 – 12322 .
  • Zhou , H , Li , J and Yang , Q . 2008 . Microbiological oxidation of sulfide chimney promoted by warm diffusing flow in CDE hydrothermal field in Eastern Lau Spreading Center . Eos Trans. AGU , 85 ( 53 ) Fall Meet. Suppl., Abstract B51D-0405
  • Zhou , J , Bruns , M and Tiedje , J . 1996 . DNA recovery from soils of diverse composition . Appl Environ Microbiol , 62 : 316 – 322 .

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.