Genome Analysis of the Biotechnologically Relevant Acidophilic Iron Oxidising Strain JA12 Indicates Phylogenetic and Metabolic Diversity within the Novel Genus “Ferrovum”

Members of the genus "Ferrovum" are ubiquitously distributed in acid mine drainage (AMD) waters which are characterised by their high metal and sulfate loads. So far isolation and microbiological characterisation have only been successful for the designated type strain "Ferrovum myxof...

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Vydané v:PloS one Ročník 11; číslo 1; s. e0146832
Hlavní autori: Ullrich, Sophie R., Poehlein, Anja, Tischler, Judith S., González, Carolina, Ossandon, Francisco J., Daniel, Rolf, Holmes, David S., Schlömann, Michael, Mühling, Martin
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States Public Library of Science 01.01.2016
Public Library of Science (PLoS)
Predmet:
Acid mine drainage
Acids
Ammonium
Bacteria
Betaproteobacteria - genetics
Bicarbonates
Bioinformatics
Biology
Biology and Life Sciences
Biotechnology
Carbon dioxide
Carbonates
Deoxyribonucleic acid
DNA
DNA, Bacterial - genetics
Ecology and Environmental Sciences
Energy sources
Evolution
Genome, Bacterial
Genomes
Genomics
Iron
Iron - metabolism
Laboratories
Leukocytes (neutrophilic)
Metabolism
Metagenome
Mining
Mixed culture
Nucleotide sequence
Nutrient uptake
Oxidation
Phosphates
Phylogenetics
Phylogeny
Physical Sciences
Proteins
Research and Analysis Methods
Rusticyanin
Sulfates
Sulfur
Thiobacillus denitrificans
Tricarboxylic acid cycle
Urea
Chile
Germany
ISSN:1932-6203, 1932-6203
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Abstract Members of the genus "Ferrovum" are ubiquitously distributed in acid mine drainage (AMD) waters which are characterised by their high metal and sulfate loads. So far isolation and microbiological characterisation have only been successful for the designated type strain "Ferrovum myxofaciens" P3G. Thus, knowledge about physiological characteristics and the phylogeny of the genus "Ferrovum" is extremely scarce. In order to access the wider genetic pool of the genus "Ferrovum" we sequenced the genome of a "Ferrovum"-containing mixed culture and successfully assembled the almost complete genome sequence of the novel "Ferrovum" strain JA12. The genome-based phylogenetic analysis indicates that strain JA12 and the type strain represent two distinct "Ferrovum" species. "Ferrovum" strain JA12 is characterised by an unusually small genome in comparison to the type strain and other iron oxidising bacteria. The prediction of nutrient assimilation pathways suggests that "Ferrovum" strain JA12 maintains a chemolithoautotrophic lifestyle utilising carbon dioxide and bicarbonate, ammonium and urea, sulfate, phosphate and ferrous iron as carbon, nitrogen, sulfur, phosphorous and energy sources, respectively. The potential utilisation of urea by "Ferrovum" strain JA12 is moreover remarkable since it may furthermore represent a strategy among extreme acidophiles to cope with the acidic environment. Unlike other acidophilic chemolithoautotrophs "Ferrovum" strain JA12 exhibits a complete tricarboxylic acid cycle, a metabolic feature shared with the closer related neutrophilic iron oxidisers among the Betaproteobacteria including Sideroxydans lithotrophicus and Thiobacillus denitrificans. Furthermore, the absence of characteristic redox proteins involved in iron oxidation in the well-studied acidophiles Acidithiobacillus ferrooxidans (rusticyanin) and Acidithiobacillus ferrivorans (iron oxidase) indicates the existence of a modified pathway in "Ferrovum" strain JA12. Therefore, the results of the present study extend our understanding of the genus "Ferrovum" and provide a comprehensive framework for future comparative genome and metagenome studies.
AbstractList Members of the genus "Ferrovum" are ubiquitously distributed in acid mine drainage (AMD) waters which are characterised by their high metal and sulfate loads. So far isolation and microbiological characterisation have only been successful for the designated type strain "Ferrovum myxofaciens" P3G. Thus, knowledge about physiological characteristics and the phylogeny of the genus "Ferrovum" is extremely scarce. In order to access the wider genetic pool of the genus "Ferrovum" we sequenced the genome of a "Ferrovum"-containing mixed culture and successfully assembled the almost complete genome sequence of the novel "Ferrovum" strain JA12. The genome-based phylogenetic analysis indicates that strain JA12 and the type strain represent two distinct "Ferrovum" species. "Ferrovum" strain JA12 is characterised by an unusually small genome in comparison to the type strain and other iron oxidising bacteria. The prediction of nutrient assimilation pathways suggests that "Ferrovum" strain JA12 maintains a chemolithoautotrophic lifestyle utilising carbon dioxide and bicarbonate, ammonium and urea, sulfate, phosphate and ferrous iron as carbon, nitrogen, sulfur, phosphorous and energy sources, respectively. The potential utilisation of urea by "Ferrovum" strain JA12 is moreover remarkable since it may furthermore represent a strategy among extreme acidophiles to cope with the acidic environment. Unlike other acidophilic chemolithoautotrophs "Ferrovum" strain JA12 exhibits a complete tricarboxylic acid cycle, a metabolic feature shared with the closer related neutrophilic iron oxidisers among the Betaproteobacteria including Sideroxydans lithotrophicus and Thiobacillus denitrificans. Furthermore, the absence of characteristic redox proteins involved in iron oxidation in the well-studied acidophiles Acidithiobacillus ferrooxidans (rusticyanin) and Acidithiobacillus ferrivorans (iron oxidase) indicates the existence of a modified pathway in "Ferrovum" strain JA12. Therefore, the results of the present study extend our understanding of the genus "Ferrovum" and provide a comprehensive framework for future comparative genome and metagenome studies.
Background Members of the genus “Ferrovum” are ubiquitously distributed in acid mine drainage (AMD) waters which are characterised by their high metal and sulfate loads. So far isolation and microbiological characterisation have only been successful for the designated type strain “Ferrovum myxofaciens” P3G. Thus, knowledge about physiological characteristics and the phylogeny of the genus “Ferrovum” is extremely scarce. Objective In order to access the wider genetic pool of the genus “Ferrovum” we sequenced the genome of a “Ferrovum”-containing mixed culture and successfully assembled the almost complete genome sequence of the novel “Ferrovum” strain JA12. Phylogeny and Lifestyle The genome-based phylogenetic analysis indicates that strain JA12 and the type strain represent two distinct “Ferrovum” species. “Ferrovum” strain JA12 is characterised by an unusually small genome in comparison to the type strain and other iron oxidising bacteria. The prediction of nutrient assimilation pathways suggests that “Ferrovum” strain JA12 maintains a chemolithoautotrophic lifestyle utilising carbon dioxide and bicarbonate, ammonium and urea, sulfate, phosphate and ferrous iron as carbon, nitrogen, sulfur, phosphorous and energy sources, respectively. Unique Metabolic Features The potential utilisation of urea by “Ferrovum” strain JA12 is moreover remarkable since it may furthermore represent a strategy among extreme acidophiles to cope with the acidic environment. Unlike other acidophilic chemolithoautotrophs “Ferrovum” strain JA12 exhibits a complete tricarboxylic acid cycle, a metabolic feature shared with the closer related neutrophilic iron oxidisers among the Betaproteobacteria including Sideroxydans lithotrophicus and Thiobacillus denitrificans. Furthermore, the absence of characteristic redox proteins involved in iron oxidation in the well-studied acidophiles Acidithiobacillus ferrooxidans (rusticyanin) and Acidithiobacillus ferrivorans (iron oxidase) indicates the existence of a modified pathway in “Ferrovum” strain JA12. Therefore, the results of the present study extend our understanding of the genus “Ferrovum” and provide a comprehensive framework for future comparative genome and metagenome studies.
BACKGROUNDMembers of the genus "Ferrovum" are ubiquitously distributed in acid mine drainage (AMD) waters which are characterised by their high metal and sulfate loads. So far isolation and microbiological characterisation have only been successful for the designated type strain "Ferrovum myxofaciens" P3G. Thus, knowledge about physiological characteristics and the phylogeny of the genus "Ferrovum" is extremely scarce.OBJECTIVEIn order to access the wider genetic pool of the genus "Ferrovum" we sequenced the genome of a "Ferrovum"-containing mixed culture and successfully assembled the almost complete genome sequence of the novel "Ferrovum" strain JA12.PHYLOGENY AND LIFESTYLEThe genome-based phylogenetic analysis indicates that strain JA12 and the type strain represent two distinct "Ferrovum" species. "Ferrovum" strain JA12 is characterised by an unusually small genome in comparison to the type strain and other iron oxidising bacteria. The prediction of nutrient assimilation pathways suggests that "Ferrovum" strain JA12 maintains a chemolithoautotrophic lifestyle utilising carbon dioxide and bicarbonate, ammonium and urea, sulfate, phosphate and ferrous iron as carbon, nitrogen, sulfur, phosphorous and energy sources, respectively.UNIQUE METABOLIC FEATURESThe potential utilisation of urea by "Ferrovum" strain JA12 is moreover remarkable since it may furthermore represent a strategy among extreme acidophiles to cope with the acidic environment. Unlike other acidophilic chemolithoautotrophs "Ferrovum" strain JA12 exhibits a complete tricarboxylic acid cycle, a metabolic feature shared with the closer related neutrophilic iron oxidisers among the Betaproteobacteria including Sideroxydans lithotrophicus and Thiobacillus denitrificans. Furthermore, the absence of characteristic redox proteins involved in iron oxidation in the well-studied acidophiles Acidithiobacillus ferrooxidans (rusticyanin) and Acidithiobacillus ferrivorans (iron oxidase) indicates the existence of a modified pathway in "Ferrovum" strain JA12. Therefore, the results of the present study extend our understanding of the genus "Ferrovum" and provide a comprehensive framework for future comparative genome and metagenome studies.
Background Members of the genus “ Ferrovum ” are ubiquitously distributed in acid mine drainage (AMD) waters which are characterised by their high metal and sulfate loads. So far isolation and microbiological characterisation have only been successful for the designated type strain “ Ferrovum myxofaciens ” P3G. Thus, knowledge about physiological characteristics and the phylogeny of the genus “ Ferrovum ” is extremely scarce. Objective In order to access the wider genetic pool of the genus “ Ferrovum ” we sequenced the genome of a “ Ferrovum ”-containing mixed culture and successfully assembled the almost complete genome sequence of the novel “ Ferrovum ” strain JA12. Phylogeny and Lifestyle The genome-based phylogenetic analysis indicates that strain JA12 and the type strain represent two distinct “ Ferrovum ” species. “ Ferrovum ” strain JA12 is characterised by an unusually small genome in comparison to the type strain and other iron oxidising bacteria. The prediction of nutrient assimilation pathways suggests that “ Ferrovum ” strain JA12 maintains a chemolithoautotrophic lifestyle utilising carbon dioxide and bicarbonate, ammonium and urea, sulfate, phosphate and ferrous iron as carbon, nitrogen, sulfur, phosphorous and energy sources, respectively. Unique Metabolic Features The potential utilisation of urea by “ Ferrovum ” strain JA12 is moreover remarkable since it may furthermore represent a strategy among extreme acidophiles to cope with the acidic environment. Unlike other acidophilic chemolithoautotrophs “ Ferrovum ” strain JA12 exhibits a complete tricarboxylic acid cycle, a metabolic feature shared with the closer related neutrophilic iron oxidisers among the Betaproteobacteria including Sideroxydans lithotrophicus and Thiobacillus denitrificans . Furthermore, the absence of characteristic redox proteins involved in iron oxidation in the well-studied acidophiles Acidithiobacillus ferrooxidans (rusticyanin) and Acidithiobacillus ferrivorans (iron oxidase) indicates the existence of a modified pathway in “ Ferrovum ” strain JA12. Therefore, the results of the present study extend our understanding of the genus “ Ferrovum ” and provide a comprehensive framework for future comparative genome and metagenome studies.
Author González, Carolina
Holmes, David S.
Poehlein, Anja
Mühling, Martin
Daniel, Rolf
Ossandon, Francisco J.
Schlömann, Michael
Ullrich, Sophie R.
Tischler, Judith S.
AuthorAffiliation 2 Georg-August-University Göttingen, Genomic and Applied Microbiology & Göttingen Genomics Laboratory, Grisebachstraße 8, Göttingen, Germany
University of Alberta, CANADA
3 Center for System Biotechnology, Bio-Computing Division and Applied Genetics Division, Fraunhofer Chile Research Foundation, Avenida Mariano Sánchez Fontecilla 310, Santiago, Chile, and Center for Bioinformatics and Genome Biology, Fundación Ciencia y Vida, Zañartu 1482, and Facultad de Ciencias Biologicas, Universidad Andres Bello, Avenida Los Leones 745, Santiago, Chile
4 Center for Bioinformatics and Genome Biology, Fundación Ciencia y Vida, Zañartu 1482 and Facultad de Ciencias Biologicas, Universidad Andres Bello, Avenida Los Leones 745, Santiago, Chile
1 Institute of Biological Sciences, TU Bergakademie Freiberg, Leipziger Straße 29, Freiberg, Germany
AuthorAffiliation_xml – name: 2 Georg-August-University Göttingen, Genomic and Applied Microbiology & Göttingen Genomics Laboratory, Grisebachstraße 8, Göttingen, Germany
– name: 3 Center for System Biotechnology, Bio-Computing Division and Applied Genetics Division, Fraunhofer Chile Research Foundation, Avenida Mariano Sánchez Fontecilla 310, Santiago, Chile, and Center for Bioinformatics and Genome Biology, Fundación Ciencia y Vida, Zañartu 1482, and Facultad de Ciencias Biologicas, Universidad Andres Bello, Avenida Los Leones 745, Santiago, Chile
– name: University of Alberta, CANADA
– name: 4 Center for Bioinformatics and Genome Biology, Fundación Ciencia y Vida, Zañartu 1482 and Facultad de Ciencias Biologicas, Universidad Andres Bello, Avenida Los Leones 745, Santiago, Chile
– name: 1 Institute of Biological Sciences, TU Bergakademie Freiberg, Leipziger Straße 29, Freiberg, Germany
Author_xml – sequence: 1
  givenname: Sophie R.
  surname: Ullrich
  fullname: Ullrich, Sophie R.
– sequence: 2
  givenname: Anja
  surname: Poehlein
  fullname: Poehlein, Anja
– sequence: 3
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  fullname: Tischler, Judith S.
– sequence: 4
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  surname: González
  fullname: González, Carolina
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  fullname: Ossandon, Francisco J.
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  fullname: Holmes, David S.
– sequence: 8
  givenname: Michael
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  fullname: Schlömann, Michael
– sequence: 9
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  fullname: Mühling, Martin
BackLink https://www.ncbi.nlm.nih.gov/pubmed/26808278$$D View this record in MEDLINE/PubMed
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Conceived and designed the experiments: MM SRU AP RD. Performed the experiments: SRU JST AP. Analyzed the data: SRU. Contributed reagents/materials/analysis tools: CG FJO DSH. Wrote the paper: SRU. Proposed the study: MM MS. Critical revision of the manuscript: MS MM DSH. Read and approved the final manuscript: SRU AP JST CG FJO RD DSH MS MM.
Competing Interests: The authors have declared that no competing interests exist.
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SSID ssj0053866
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Snippet Members of the genus "Ferrovum" are ubiquitously distributed in acid mine drainage (AMD) waters which are characterised by their high metal and sulfate loads....
Background Members of the genus “Ferrovum” are ubiquitously distributed in acid mine drainage (AMD) waters which are characterised by their high metal and...
BACKGROUNDMembers of the genus "Ferrovum" are ubiquitously distributed in acid mine drainage (AMD) waters which are characterised by their high metal and...
BACKGROUND:Members of the genus "Ferrovum" are ubiquitously distributed in acid mine drainage (AMD) waters which are characterised by their high metal and...
Background Members of the genus “ Ferrovum ” are ubiquitously distributed in acid mine drainage (AMD) waters which are characterised by their high metal and...
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StartPage e0146832
SubjectTerms Acid mine drainage
Acids
Ammonium
Bacteria
Betaproteobacteria - genetics
Bicarbonates
Bioinformatics
Biology
Biology and Life Sciences
Biotechnology
Carbon dioxide
Carbonates
Deoxyribonucleic acid
DNA
DNA, Bacterial - genetics
Ecology and Environmental Sciences
Energy sources
Evolution
Genome, Bacterial
Genomes
Genomics
Iron
Iron - metabolism
Laboratories
Leukocytes (neutrophilic)
Metabolism
Metagenome
Mining
Mixed culture
Nucleotide sequence
Nutrient uptake
Oxidation
Phosphates
Phylogenetics
Phylogeny
Physical Sciences
Proteins
Research and Analysis Methods
Rusticyanin
Sulfates
Sulfur
Thiobacillus denitrificans
Tricarboxylic acid cycle
Urea
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Title Genome Analysis of the Biotechnologically Relevant Acidophilic Iron Oxidising Strain JA12 Indicates Phylogenetic and Metabolic Diversity within the Novel Genus “Ferrovum”
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Volume 11
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