Methanotrophy below pH 1 by a new Verrucomicrobia species

Passing the acid test Bacteria that consume the greenhouse gas methane are potentially important players in the atmospheric budget, with the potential to sop up methane from the Earth's crust that would otherwise contribute to the atmospheric budget. Two new methane-utilizing bacteria have been...

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Veröffentlicht in:Nature 2007-12, Vol.450 (7171), p.874-878
Hauptverfasser: Pol, Arjan, Heijmans, Klaas, Harhangi, Harry R., Tedesco, Dario, Jetten, Mike S. M., Op den Camp, Huub J. M.
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container_issue 7171
container_start_page 874
container_title Nature
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creator Pol, Arjan
Heijmans, Klaas
Harhangi, Harry R.
Tedesco, Dario
Jetten, Mike S. M.
Op den Camp, Huub J. M.
description Passing the acid test Bacteria that consume the greenhouse gas methane are potentially important players in the atmospheric budget, with the potential to sop up methane from the Earth's crust that would otherwise contribute to the atmospheric budget. Two new methane-utilizing bacteria have been isolated independently and both break new ground: unlike previous methanotrophic isolates, which are proteobacteria, they belong to the widely distributed Verrucomicrobia phylum. And both isolates display optimum growth and methane oxidation in remarkably acidic conditions, at pHs as low as 0.8 to 2.5. Acidimethylosilex fumarolicum SolV was isolated from a fuming vent on the Solfatara volcano near Naples, Italy, and Methylokorus infernorum from hot soil in the Hell's Gate (Tikitere) geothermal area of New Zealand. The isolation of the acidophilic bacterium Acidimethylosilex fumarolicum SolV from a fumarole is described. Unlike all previous methanotrophic isolates, which belong to the Alpha- or Gammaproteobacteria, it belongs to the widely distributed Verrumicrobia. Mud volcanoes, mudpots and fumaroles are remarkable geological features characterized by the emission of gas, water and/or semi-liquid mud matrices 1 with significant methane fluxes to the atmosphere (10 -1 to 10 3  t y -1 ) 2 , 3 , 4 . Environmental conditions in these areas vary from ambient temperature and neutral pH to high temperatures and low pH. Although there are strong indications for biological methane consumption in mud volcanoes 4 , 5 , no methanotrophic bacteria are known that would thrive in the hostile conditions of fumaroles (temperatures up to 70 °C and pH down to 1.8) 2 . The first step in aerobic methane oxidation is performed by a soluble or membrane-bound methane mono-oxygenase. Here we report that pmoA (encoding the β-subunit of membrane-bound methane mono-oxygenase) clone libraries, made by using DNA extracted from the Solfatara volcano mudpot and surrounding bare soil near the fumaroles, showed clusters of novel and distant pmoA genes. After methanotrophic enrichment at 50 °C and pH 2.0 the most distant cluster, sharing less than 50% identity with any other described pmoA gene, was represented in the culture. Finally we isolated an acidiphilic methanotrophic bacterium Acidimethylosilex fumarolicum SolV belonging to the Planctomycetes/Verrucomicrobia/Chlamydiae superphylum 6 , ‘outside’ the subphyla of the Alpha- and Gammaproteobacteria containing the established methanotrophs. This
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M. ; Op den Camp, Huub J. M.</creator><creatorcontrib>Pol, Arjan ; Heijmans, Klaas ; Harhangi, Harry R. ; Tedesco, Dario ; Jetten, Mike S. M. ; Op den Camp, Huub J. M.</creatorcontrib><description>Passing the acid test Bacteria that consume the greenhouse gas methane are potentially important players in the atmospheric budget, with the potential to sop up methane from the Earth's crust that would otherwise contribute to the atmospheric budget. Two new methane-utilizing bacteria have been isolated independently and both break new ground: unlike previous methanotrophic isolates, which are proteobacteria, they belong to the widely distributed Verrucomicrobia phylum. And both isolates display optimum growth and methane oxidation in remarkably acidic conditions, at pHs as low as 0.8 to 2.5. Acidimethylosilex fumarolicum SolV was isolated from a fuming vent on the Solfatara volcano near Naples, Italy, and Methylokorus infernorum from hot soil in the Hell's Gate (Tikitere) geothermal area of New Zealand. The isolation of the acidophilic bacterium Acidimethylosilex fumarolicum SolV from a fumarole is described. Unlike all previous methanotrophic isolates, which belong to the Alpha- or Gammaproteobacteria, it belongs to the widely distributed Verrumicrobia. Mud volcanoes, mudpots and fumaroles are remarkable geological features characterized by the emission of gas, water and/or semi-liquid mud matrices 1 with significant methane fluxes to the atmosphere (10 -1 to 10 3  t y -1 ) 2 , 3 , 4 . Environmental conditions in these areas vary from ambient temperature and neutral pH to high temperatures and low pH. Although there are strong indications for biological methane consumption in mud volcanoes 4 , 5 , no methanotrophic bacteria are known that would thrive in the hostile conditions of fumaroles (temperatures up to 70 °C and pH down to 1.8) 2 . The first step in aerobic methane oxidation is performed by a soluble or membrane-bound methane mono-oxygenase. Here we report that pmoA (encoding the β-subunit of membrane-bound methane mono-oxygenase) clone libraries, made by using DNA extracted from the Solfatara volcano mudpot and surrounding bare soil near the fumaroles, showed clusters of novel and distant pmoA genes. After methanotrophic enrichment at 50 °C and pH 2.0 the most distant cluster, sharing less than 50% identity with any other described pmoA gene, was represented in the culture. Finally we isolated an acidiphilic methanotrophic bacterium Acidimethylosilex fumarolicum SolV belonging to the Planctomycetes/Verrucomicrobia/Chlamydiae superphylum 6 , ‘outside’ the subphyla of the Alpha- and Gammaproteobacteria containing the established methanotrophs. This bacterium grows under oxygen limitation on methane as the sole source of energy, down to pH 0.8—far below the pH optimum of any previously described methanotroph. A. fumarolicum SolV has three different pmoA genes, with two that are very similar to sequences retrieved from the mudpot. Highly homologous environmental 16S rRNA gene sequences from Yellowstone Park show that this new type of methanotrophic bacteria may be a common inhabitant of extreme environments. 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Psychology ; Gene Library ; Genes ; Genes, Bacterial - genetics ; Genetics ; Geologic Sediments - microbiology ; Geology ; High temperature ; Hot Springs - microbiology ; Hot Temperature ; Humanities and Social Sciences ; Hydrogen-Ion Concentration ; In Situ Hybridization, Fluorescence ; letter ; Membranes ; Methane ; Methane - chemistry ; Methane - metabolism ; Microbiology ; Molecular Sequence Data ; Mud ; multidisciplinary ; Oxidation ; Oxygen - analysis ; Oxygenases - genetics ; Phylogeny ; Planctomycetes ; RNA, Ribosomal, 16S - genetics ; Science ; Science (multidisciplinary) ; Verrucomicrobia ; Volcanic Eruptions ; Volcanoes</subject><ispartof>Nature, 2007-12, Vol.450 (7171), p.874-878</ispartof><rights>Springer Nature Limited 2007</rights><rights>2008 INIST-CNRS</rights><rights>COPYRIGHT 2007 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Dec 6, 2007</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c8322-eb27a559821619c28c5fda0866c73a8568695e84a4be45db4e7bf0cfbe5b016a3</citedby><cites>FETCH-LOGICAL-c8322-eb27a559821619c28c5fda0866c73a8568695e84a4be45db4e7bf0cfbe5b016a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/nature06222$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/nature06222$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=19868809$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18004305$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Pol, Arjan</creatorcontrib><creatorcontrib>Heijmans, Klaas</creatorcontrib><creatorcontrib>Harhangi, Harry R.</creatorcontrib><creatorcontrib>Tedesco, Dario</creatorcontrib><creatorcontrib>Jetten, Mike S. M.</creatorcontrib><creatorcontrib>Op den Camp, Huub J. M.</creatorcontrib><title>Methanotrophy below pH 1 by a new Verrucomicrobia species</title><title>Nature</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>Passing the acid test Bacteria that consume the greenhouse gas methane are potentially important players in the atmospheric budget, with the potential to sop up methane from the Earth's crust that would otherwise contribute to the atmospheric budget. Two new methane-utilizing bacteria have been isolated independently and both break new ground: unlike previous methanotrophic isolates, which are proteobacteria, they belong to the widely distributed Verrucomicrobia phylum. And both isolates display optimum growth and methane oxidation in remarkably acidic conditions, at pHs as low as 0.8 to 2.5. Acidimethylosilex fumarolicum SolV was isolated from a fuming vent on the Solfatara volcano near Naples, Italy, and Methylokorus infernorum from hot soil in the Hell's Gate (Tikitere) geothermal area of New Zealand. The isolation of the acidophilic bacterium Acidimethylosilex fumarolicum SolV from a fumarole is described. Unlike all previous methanotrophic isolates, which belong to the Alpha- or Gammaproteobacteria, it belongs to the widely distributed Verrumicrobia. Mud volcanoes, mudpots and fumaroles are remarkable geological features characterized by the emission of gas, water and/or semi-liquid mud matrices 1 with significant methane fluxes to the atmosphere (10 -1 to 10 3  t y -1 ) 2 , 3 , 4 . Environmental conditions in these areas vary from ambient temperature and neutral pH to high temperatures and low pH. Although there are strong indications for biological methane consumption in mud volcanoes 4 , 5 , no methanotrophic bacteria are known that would thrive in the hostile conditions of fumaroles (temperatures up to 70 °C and pH down to 1.8) 2 . The first step in aerobic methane oxidation is performed by a soluble or membrane-bound methane mono-oxygenase. Here we report that pmoA (encoding the β-subunit of membrane-bound methane mono-oxygenase) clone libraries, made by using DNA extracted from the Solfatara volcano mudpot and surrounding bare soil near the fumaroles, showed clusters of novel and distant pmoA genes. After methanotrophic enrichment at 50 °C and pH 2.0 the most distant cluster, sharing less than 50% identity with any other described pmoA gene, was represented in the culture. Finally we isolated an acidiphilic methanotrophic bacterium Acidimethylosilex fumarolicum SolV belonging to the Planctomycetes/Verrucomicrobia/Chlamydiae superphylum 6 , ‘outside’ the subphyla of the Alpha- and Gammaproteobacteria containing the established methanotrophs. This bacterium grows under oxygen limitation on methane as the sole source of energy, down to pH 0.8—far below the pH optimum of any previously described methanotroph. A. fumarolicum SolV has three different pmoA genes, with two that are very similar to sequences retrieved from the mudpot. Highly homologous environmental 16S rRNA gene sequences from Yellowstone Park show that this new type of methanotrophic bacteria may be a common inhabitant of extreme environments. 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Transportation Engineering Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>METADEX</collection><collection>ANTE: Abstracts in New Technology &amp; Engineering</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts – Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science &amp; Fisheries Abstracts (ASFA) 1: Biological Sciences &amp; Living Resources</collection><collection>Aquatic Science &amp; Fisheries Abstracts (ASFA) 2: Ocean Technology, Policy &amp; Non-Living Resources</collection><collection>Aquatic Science &amp; Fisheries Abstracts (ASFA) Professional</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>MEDLINE - Academic</collection><jtitle>Nature</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pol, Arjan</au><au>Heijmans, Klaas</au><au>Harhangi, Harry R.</au><au>Tedesco, Dario</au><au>Jetten, Mike S. M.</au><au>Op den Camp, Huub J. M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Methanotrophy below pH 1 by a new Verrucomicrobia species</atitle><jtitle>Nature</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2007-12-06</date><risdate>2007</risdate><volume>450</volume><issue>7171</issue><spage>874</spage><epage>878</epage><pages>874-878</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><eissn>1476-4679</eissn><coden>NATUAS</coden><abstract>Passing the acid test Bacteria that consume the greenhouse gas methane are potentially important players in the atmospheric budget, with the potential to sop up methane from the Earth's crust that would otherwise contribute to the atmospheric budget. Two new methane-utilizing bacteria have been isolated independently and both break new ground: unlike previous methanotrophic isolates, which are proteobacteria, they belong to the widely distributed Verrucomicrobia phylum. And both isolates display optimum growth and methane oxidation in remarkably acidic conditions, at pHs as low as 0.8 to 2.5. Acidimethylosilex fumarolicum SolV was isolated from a fuming vent on the Solfatara volcano near Naples, Italy, and Methylokorus infernorum from hot soil in the Hell's Gate (Tikitere) geothermal area of New Zealand. The isolation of the acidophilic bacterium Acidimethylosilex fumarolicum SolV from a fumarole is described. Unlike all previous methanotrophic isolates, which belong to the Alpha- or Gammaproteobacteria, it belongs to the widely distributed Verrumicrobia. Mud volcanoes, mudpots and fumaroles are remarkable geological features characterized by the emission of gas, water and/or semi-liquid mud matrices 1 with significant methane fluxes to the atmosphere (10 -1 to 10 3  t y -1 ) 2 , 3 , 4 . Environmental conditions in these areas vary from ambient temperature and neutral pH to high temperatures and low pH. Although there are strong indications for biological methane consumption in mud volcanoes 4 , 5 , no methanotrophic bacteria are known that would thrive in the hostile conditions of fumaroles (temperatures up to 70 °C and pH down to 1.8) 2 . The first step in aerobic methane oxidation is performed by a soluble or membrane-bound methane mono-oxygenase. Here we report that pmoA (encoding the β-subunit of membrane-bound methane mono-oxygenase) clone libraries, made by using DNA extracted from the Solfatara volcano mudpot and surrounding bare soil near the fumaroles, showed clusters of novel and distant pmoA genes. After methanotrophic enrichment at 50 °C and pH 2.0 the most distant cluster, sharing less than 50% identity with any other described pmoA gene, was represented in the culture. Finally we isolated an acidiphilic methanotrophic bacterium Acidimethylosilex fumarolicum SolV belonging to the Planctomycetes/Verrucomicrobia/Chlamydiae superphylum 6 , ‘outside’ the subphyla of the Alpha- and Gammaproteobacteria containing the established methanotrophs. This bacterium grows under oxygen limitation on methane as the sole source of energy, down to pH 0.8—far below the pH optimum of any previously described methanotroph. A. fumarolicum SolV has three different pmoA genes, with two that are very similar to sequences retrieved from the mudpot. Highly homologous environmental 16S rRNA gene sequences from Yellowstone Park show that this new type of methanotrophic bacteria may be a common inhabitant of extreme environments. This is the first time that a representative of the widely distributed Verrucomicrobia phylum, of which most members remain uncultivated 6 , is coupled to a geochemically relevant reaction.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>18004305</pmid><doi>10.1038/nature06222</doi><tpages>5</tpages></addata></record>
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identifier ISSN: 0028-0836
ispartof Nature, 2007-12, Vol.450 (7171), p.874-878
issn 0028-0836
1476-4687
1476-4679
language eng
recordid cdi_proquest_miscellaneous_743308032
source MEDLINE; SpringerLink Journals; Nature Journals Online
subjects Acids - analysis
Acids - chemistry
Ambient temperature
Atmosphere
Bacteria
Bacteria - classification
Bacteria - enzymology
Bacteria - genetics
Bacteria - metabolism
Bacterial Proteins - chemistry
Bacterial Proteins - genetics
Bacteriology
Biological and medical sciences
Clusters
Deoxyribonucleic acid
DNA
Emissions
Environmental conditions
Fumaroles
Fundamental and applied biological sciences. Psychology
Gene Library
Genes
Genes, Bacterial - genetics
Genetics
Geologic Sediments - microbiology
Geology
High temperature
Hot Springs - microbiology
Hot Temperature
Humanities and Social Sciences
Hydrogen-Ion Concentration
In Situ Hybridization, Fluorescence
letter
Membranes
Methane
Methane - chemistry
Methane - metabolism
Microbiology
Molecular Sequence Data
Mud
multidisciplinary
Oxidation
Oxygen - analysis
Oxygenases - genetics
Phylogeny
Planctomycetes
RNA, Ribosomal, 16S - genetics
Science
Science (multidisciplinary)
Verrucomicrobia
Volcanic Eruptions
Volcanoes
title Methanotrophy below pH 1 by a new Verrucomicrobia species
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