Complete genome, catabolic sub-proteomes and key-metabolites of Desulfobacula toluolica Tol2, a marine, aromatic compound-degrading, sulfate-reducing bacterium

Summary Among the dominant deltaproteobacterial sulfate‐reducing bacteria (SRB), members of the genus Desulfobacula are not only present in (hydrocarbon‐rich) marine sediments, but occur also frequently in the anoxic water bodies encountered in marine upwelling areas. Here, we present the 5.2 Mbp ge...

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Published in:	Environmental microbiology Vol. 15; no. 5; pp. 1334 - 1355
Main Authors:	Wöhlbrand, Lars, Jacob, Jacob H., Kube, Michael, Mussmann, Marc, Jarling, René, Beck, Alfred, Amann, Rudolf, Wilkes, Heinz, Reinhardt, Richard, Rabus, Ralf
Format:	Journal Article
Language:	English
Published:	England Blackwell Publishing Ltd 01.05.2013
Subjects:	Deltaproteobacteria - classification Deltaproteobacteria - genetics Deltaproteobacteria - metabolism Deltaproteobacteria - virology Energy Metabolism - genetics Gene Expression Regulation, Bacterial Genes, Bacterial - genetics Genome, Bacterial Metabolic Networks and Pathways - genetics Metabolism - genetics Phylogeny Proteome Signal Transduction Stress, Physiological - genetics
ISSN:	1462-2912, 1462-2920, 1462-2920
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Abstract	Summary Among the dominant deltaproteobacterial sulfate‐reducing bacteria (SRB), members of the genus Desulfobacula are not only present in (hydrocarbon‐rich) marine sediments, but occur also frequently in the anoxic water bodies encountered in marine upwelling areas. Here, we present the 5.2 Mbp genome of Desulfobacula toluolica Tol2, which is the first of an aromatic compound‐degrading, marine SRB. The genome has apparently been shaped by viral attacks (e.g. CRISPRs) and its high plasticity is reflected by 163 detected genes related to transposases and integrases, a total of 494 paralogous genes and 24 group II introns. Prediction of the catabolic network of strain Tol2 was refined by differential proteome and metabolite analysis of substrate‐adapted cells. Toluene and p‐cresol are degraded by separate suites of specific enzymes for initial arylsuccinate formation via addition to fumarate (p‐cresol‐specific enzyme HbsA represents a new phylogenetic branch) as well as for subsequent modified β‐oxidation of arylsuccinates to the central intermediate benzoyl‐CoA. Proteogenomic evidence suggests specific electron transfer (EtfAB) and membrane proteins to channel electrons from dehydrogenation of both arylsuccinates directly to the membrane redox pool. In contrast to the known anaerobic degradation pathways in other bacteria, strain Tol2 deaminates phenylalanine non‐oxidatively to cinnamate by phenylalanine ammonia‐lyase and subsequently forms phenylacetate (both metabolites identified in 13C‐labelling experiments). Benzoate degradation involves CoA activation, reductive dearomatization by a class II benzoyl‐CoA reductase and hydrolytic ring cleavage as found in the obligate anaerobe Geobacter metallireducens GS‐15. The catabolic sub‐proteomes displayed high substrate specificity, reflecting the genomically predicted complex and fine‐tuned regulatory network of strain Tol2. Despite the genetic equipment for a TCA cycle, proteomic evidence supports complete oxidation of acetyl‐CoA to CO2 via the Wood‐Ljungdahl pathway. Strain Tol2 possesses transmembrane redox complexes similar to that of other Desulfobacteraceae members. The multiple heterodisulfide reductase‐like proteins (more than described for Desulfobacterium autotrophicum HRM2) may constitute a multifaceted cytoplasmic electron transfer network.
AbstractList	Among the dominant deltaproteobacterial sulfate-reducing bacteria (SRB), members of the genus Desulfobacula are not only present in (hydrocarbon-rich) marine sediments, but occur also frequently in the anoxic water bodies encountered in marine upwelling areas. Here, we present the 5.2 Mbp genome of Desulfobacula toluolica Tol2, which is the first of an aromatic compound-degrading, marine SRB. The genome has apparently been shaped by viral attacks (e.g. CRISPRs) and its high plasticity is reflected by 163 detected genes related to transposases and integrases, a total of 494 paralogous genes and 24 group II introns. Prediction of the catabolic network of strain Tol2 was refined by differential proteome and metabolite analysis of substrate-adapted cells. Toluene and p-cresol are degraded by separate suites of specific enzymes for initial arylsuccinate formation via addition to fumarate (p-cresol-specific enzyme HbsA represents a new phylogenetic branch) as well as for subsequent modified β-oxidation of arylsuccinates to the central intermediate benzoyl-CoA. Proteogenomic evidence suggests specific electron transfer (EtfAB) and membrane proteins to channel electrons from dehydrogenation of both arylsuccinates directly to the membrane redox pool. In contrast to the known anaerobic degradation pathways in other bacteria, strain Tol2 deaminates phenylalanine non-oxidatively to cinnamate by phenylalanine ammonia-lyase and subsequently forms phenylacetate (both metabolites identified in (13) C-labelling experiments). Benzoate degradation involves CoA activation, reductive dearomatization by a class II benzoyl-CoA reductase and hydrolytic ring cleavage as found in the obligate anaerobe Geobacter metallireducens GS-15. The catabolic sub-proteomes displayed high substrate specificity, reflecting the genomically predicted complex and fine-tuned regulatory network of strain Tol2. Despite the genetic equipment for a TCA cycle, proteomic evidence supports complete oxidation of acetyl-CoA to CO2 via the Wood-Ljungdahl pathway. Strain Tol2 possesses transmembrane redox complexes similar to that of other Desulfobacteraceae members. The multiple heterodisulfide reductase-like proteins (more than described for Desulfobacterium autotrophicum HRM2) may constitute a multifaceted cytoplasmic electron transfer network.Among the dominant deltaproteobacterial sulfate-reducing bacteria (SRB), members of the genus Desulfobacula are not only present in (hydrocarbon-rich) marine sediments, but occur also frequently in the anoxic water bodies encountered in marine upwelling areas. Here, we present the 5.2 Mbp genome of Desulfobacula toluolica Tol2, which is the first of an aromatic compound-degrading, marine SRB. The genome has apparently been shaped by viral attacks (e.g. CRISPRs) and its high plasticity is reflected by 163 detected genes related to transposases and integrases, a total of 494 paralogous genes and 24 group II introns. Prediction of the catabolic network of strain Tol2 was refined by differential proteome and metabolite analysis of substrate-adapted cells. Toluene and p-cresol are degraded by separate suites of specific enzymes for initial arylsuccinate formation via addition to fumarate (p-cresol-specific enzyme HbsA represents a new phylogenetic branch) as well as for subsequent modified β-oxidation of arylsuccinates to the central intermediate benzoyl-CoA. Proteogenomic evidence suggests specific electron transfer (EtfAB) and membrane proteins to channel electrons from dehydrogenation of both arylsuccinates directly to the membrane redox pool. In contrast to the known anaerobic degradation pathways in other bacteria, strain Tol2 deaminates phenylalanine non-oxidatively to cinnamate by phenylalanine ammonia-lyase and subsequently forms phenylacetate (both metabolites identified in (13) C-labelling experiments). Benzoate degradation involves CoA activation, reductive dearomatization by a class II benzoyl-CoA reductase and hydrolytic ring cleavage as found in the obligate anaerobe Geobacter metallireducens GS-15. The catabolic sub-proteomes displayed high substrate specificity, reflecting the genomically predicted complex and fine-tuned regulatory network of strain Tol2. Despite the genetic equipment for a TCA cycle, proteomic evidence supports complete oxidation of acetyl-CoA to CO2 via the Wood-Ljungdahl pathway. Strain Tol2 possesses transmembrane redox complexes similar to that of other Desulfobacteraceae members. The multiple heterodisulfide reductase-like proteins (more than described for Desulfobacterium autotrophicum HRM2) may constitute a multifaceted cytoplasmic electron transfer network. Among the dominant deltaproteobacterial sulfate-reducing bacteria (SRB), members of the genus Desulfobacula are not only present in (hydrocarbon-rich) marine sediments, but occur also frequently in the anoxic water bodies encountered in marine upwelling areas. Here, we present the 5.2 Mbp genome of Desulfobacula toluolica Tol2, which is the first of an aromatic compound-degrading, marine SRB. The genome has apparently been shaped by viral attacks (e.g. CRISPRs) and its high plasticity is reflected by 163 detected genes related to transposases and integrases, a total of 494 paralogous genes and 24 group II introns. Prediction of the catabolic network of strain Tol2 was refined by differential proteome and metabolite analysis of substrate-adapted cells. Toluene and p-cresol are degraded by separate suites of specific enzymes for initial arylsuccinate formation via addition to fumarate (p-cresol-specific enzyme HbsA represents a new phylogenetic branch) as well as for subsequent modified β-oxidation of arylsuccinates to the central intermediate benzoyl-CoA. Proteogenomic evidence suggests specific electron transfer (EtfAB) and membrane proteins to channel electrons from dehydrogenation of both arylsuccinates directly to the membrane redox pool. In contrast to the known anaerobic degradation pathways in other bacteria, strain Tol2 deaminates phenylalanine non-oxidatively to cinnamate by phenylalanine ammonia-lyase and subsequently forms phenylacetate (both metabolites identified in (13) C-labelling experiments). Benzoate degradation involves CoA activation, reductive dearomatization by a class II benzoyl-CoA reductase and hydrolytic ring cleavage as found in the obligate anaerobe Geobacter metallireducens GS-15. The catabolic sub-proteomes displayed high substrate specificity, reflecting the genomically predicted complex and fine-tuned regulatory network of strain Tol2. Despite the genetic equipment for a TCA cycle, proteomic evidence supports complete oxidation of acetyl-CoA to CO2 via the Wood-Ljungdahl pathway. Strain Tol2 possesses transmembrane redox complexes similar to that of other Desulfobacteraceae members. The multiple heterodisulfide reductase-like proteins (more than described for Desulfobacterium autotrophicum HRM2) may constitute a multifaceted cytoplasmic electron transfer network. Summary Among the dominant deltaproteobacterial sulfate‐reducing bacteria (SRB), members of the genus Desulfobacula are not only present in (hydrocarbon‐rich) marine sediments, but occur also frequently in the anoxic water bodies encountered in marine upwelling areas. Here, we present the 5.2 Mbp genome of Desulfobacula toluolica Tol2, which is the first of an aromatic compound‐degrading, marine SRB. The genome has apparently been shaped by viral attacks (e.g. CRISPRs) and its high plasticity is reflected by 163 detected genes related to transposases and integrases, a total of 494 paralogous genes and 24 group II introns. Prediction of the catabolic network of strain Tol2 was refined by differential proteome and metabolite analysis of substrate‐adapted cells. Toluene and p‐cresol are degraded by separate suites of specific enzymes for initial arylsuccinate formation via addition to fumarate (p‐cresol‐specific enzyme HbsA represents a new phylogenetic branch) as well as for subsequent modified β‐oxidation of arylsuccinates to the central intermediate benzoyl‐CoA. Proteogenomic evidence suggests specific electron transfer (EtfAB) and membrane proteins to channel electrons from dehydrogenation of both arylsuccinates directly to the membrane redox pool. In contrast to the known anaerobic degradation pathways in other bacteria, strain Tol2 deaminates phenylalanine non‐oxidatively to cinnamate by phenylalanine ammonia‐lyase and subsequently forms phenylacetate (both metabolites identified in 13C‐labelling experiments). Benzoate degradation involves CoA activation, reductive dearomatization by a class II benzoyl‐CoA reductase and hydrolytic ring cleavage as found in the obligate anaerobe Geobacter metallireducens GS‐15. The catabolic sub‐proteomes displayed high substrate specificity, reflecting the genomically predicted complex and fine‐tuned regulatory network of strain Tol2. Despite the genetic equipment for a TCA cycle, proteomic evidence supports complete oxidation of acetyl‐CoA to CO2 via the Wood‐Ljungdahl pathway. Strain Tol2 possesses transmembrane redox complexes similar to that of other Desulfobacteraceae members. The multiple heterodisulfide reductase‐like proteins (more than described for Desulfobacterium autotrophicum HRM2) may constitute a multifaceted cytoplasmic electron transfer network.
Author	Rabus, Ralf Jacob, Jacob H. Kube, Michael Jarling, René Beck, Alfred Wöhlbrand, Lars Wilkes, Heinz Reinhardt, Richard Mussmann, Marc Amann, Rudolf
Author_xml	– sequence: 1 givenname: Lars surname: Wöhlbrand fullname: Wöhlbrand, Lars organization: Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl von Ossietzky University Oldenburg, Carl-von-Ossietzky-Strasse 9-11, 26111, Oldenburg, Germany – sequence: 2 givenname: Jacob H. surname: Jacob fullname: Jacob, Jacob H. organization: Max-Planck-Institute for Marine Microbiology, Celsiusstrasse 1, 28359, Bremen, Germany – sequence: 3 givenname: Michael surname: Kube fullname: Kube, Michael organization: Max-Planck-Institute for Molecular Genetics, Ihnestrasse 63-73, 14195, Berlin, Germany – sequence: 4 givenname: Marc surname: Mussmann fullname: Mussmann, Marc organization: Max-Planck-Institute for Marine Microbiology, Celsiusstrasse 1, 28359, Bremen, Germany – sequence: 5 givenname: René surname: Jarling fullname: Jarling, René organization: Helmholtz Centre Potsdam GFZ German Research Centre for Geosciences, Telegrafenberg, 14473, Potsdam, Germany – sequence: 6 givenname: Alfred surname: Beck fullname: Beck, Alfred organization: Max-Planck-Institute for Molecular Genetics, Ihnestrasse 63-73, 14195, Berlin, Germany – sequence: 7 givenname: Rudolf surname: Amann fullname: Amann, Rudolf organization: Max-Planck-Institute for Marine Microbiology, Celsiusstrasse 1, 28359, Bremen, Germany – sequence: 8 givenname: Heinz surname: Wilkes fullname: Wilkes, Heinz organization: Helmholtz Centre Potsdam GFZ German Research Centre for Geosciences, Telegrafenberg, 14473, Potsdam, Germany – sequence: 9 givenname: Richard surname: Reinhardt fullname: Reinhardt, Richard organization: Max-Planck-Institute for Molecular Genetics, Ihnestrasse 63-73, 14195, Berlin, Germany – sequence: 10 givenname: Ralf surname: Rabus fullname: Rabus, Ralf email: rabus@icbm.de organization: Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl von Ossietzky University Oldenburg, Carl-von-Ossietzky-Strasse 9-11, 26111, Oldenburg, Germany
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Notes	University of Oldenburg ark:/67375/WNG-JRNMHWZ9-B Catabolic network. Table S1. Selected identified proteins. Fig. S1. False-colour images of 2D DIGE gels. Fig. S2. Phylogenetic relations and gene clusters of class II benzoyl-CoA reductases. Fig. S3. Scale model of gene clusters related to anaerobic phenylacetate catabolism. Fig. S4. Scale model of the gene cluster related to anaerobic phenol catabolism. Fig. S5. Scale model of the conserved gene clusters encoding enzymes of the Wood-Ljungdahl pathway in SRB. Fig. S6. Scale model of gene clusters containing hdlA genes of strain Tol2 according to hdlA phylogenetic relation. Max-Planck Society istex:458F14AB2730AB27BB2EB9B40437639418A77442 ArticleID:EMI2885 ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
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Snippet	Summary Among the dominant deltaproteobacterial sulfate‐reducing bacteria (SRB), members of the genus Desulfobacula are not only present in (hydrocarbon‐rich)... Among the dominant deltaproteobacterial sulfate-reducing bacteria (SRB), members of the genus Desulfobacula are not only present in (hydrocarbon-rich) marine...
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SubjectTerms	Deltaproteobacteria - classification Deltaproteobacteria - genetics Deltaproteobacteria - metabolism Deltaproteobacteria - virology Energy Metabolism - genetics Gene Expression Regulation, Bacterial Genes, Bacterial - genetics Genome, Bacterial Metabolic Networks and Pathways - genetics Metabolism - genetics Phylogeny Proteome Signal Transduction Stress, Physiological - genetics
Title	Complete genome, catabolic sub-proteomes and key-metabolites of Desulfobacula toluolica Tol2, a marine, aromatic compound-degrading, sulfate-reducing bacterium
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