Unravelling the complete genome sequence of Advenella mimigardefordensis strain DPN7T and novel insights in the catabolism of the xenobiotic polythioester precursor 3,3'-dithiodipropionate.

Advenella mimigardefordensis strain DPN7(T) is a remarkable betaproteobacterium because of its extraordinary ability to use the synthetic disulfide 3,3'-dithiodipropionic acid (DTDP) as the sole carbon source and electron donor for aerobic growth. One application of DTDP is as a precursor substrate for biotechnically synthesized polythioesters (PTEs), which are interesting non-degradable biopolymers applicable for plastics materials. Metabolic engineering for optimization of PTE production requires an understanding of DTDP conversion. The genome of A. mimigardefordensis strain DPN7(T) was sequenced and annotated. The circular chromosome was found to be composed of 4,740,516 bp and 4112 predicted ORFs, whereas the circular plasmid consisted of 23,610 bp and 24 predicted ORFs. The genes participating in DTDP catabolism had been characterized in detail previously, but knowing the complete genome sequence and with support of Tn5: :mob-induced mutants, putatively involved transporter proteins and a transcriptional regulator were also identified. Most probably, DTDP is transported into the cell by a specific tripartite tricarboxylate transport system and is then cleaved by the disulfide reductase LpdA, sulfoxygenated by the 3-mercaptopropionate dioxygenase Mdo, activated by the CoA ligase SucCD and desulfinated by the acyl-CoA dehydrogenase-like desulfinase AcdA. Regulation of this pathway is presumably performed by a transcriptional regulator of the xenobiotic response element family. The excessive sulfate that is inevitably produced is secreted by the cells by a unique sulfate exporter of the CPA (cation : proton antiporter) superfamily.

[1]  U. Kappler,et al.  Sulfite-oxidizing enzymes , 2015, JBIC Journal of Biological Inorganic Chemistry.

[2]  A. Deters,et al.  A Novel 3-Sulfinopropionyl Coenzyme A (3SP-CoA) Desulfinase from Advenella mimigardefordensis Strain DPN7T Acting as a Key Enzyme during Catabolism of 3,3′-Dithiodipropionic Acid Is a Member of the Acyl-CoA Dehydrogenase Superfamily , 2013, Journal of bacteriology.

[3]  K. Kamino,et al.  Advenella faeciporci sp. nov., a nitrite-denitrifying bacterium isolated from nitrifying-denitrifying activated sludge collected from a laboratory-scale bioreactor treating piggery wastewater. , 2012, International journal of systematic and evolutionary microbiology.

[4]  E. Cascales,et al.  Structure and regulation of the type VI secretion system. , 2012, Annual review of microbiology.

[5]  D. Schleheck,et al.  (R)-Cysteate-nitrogen assimilation by Cupriavidus necator H16 with excretion of 3-sulfolactate: a patchwork pathway , 2012, Archives of Microbiology.

[6]  A. Sinskey,et al.  Examination of PHB Depolymerases in Ralstonia eutropha: Further Elucidation of the Roles of Enzymes in PHB Homeostasis , 2012, AMB Express.

[7]  H. Dobbek,et al.  The Fe(II)/α‐ketoglutarate‐dependent taurine dioxygenases from Pseudomonas putida and Escherichia coli are tetramers , 2012, The FEBS journal.

[8]  A. Steinbüchel,et al.  Employing a Recombinant Strain of Advenella mimigardefordensis for Biotechnical Production of Homopolythioesters from 3,3′-Dithiodipropionic Acid , 2012, Applied and Environmental Microbiology.

[9]  Peter Williams,et al.  IMG: the integrated microbial genomes database and comparative analysis system , 2011, Nucleic Acids Res..

[10]  A. Wagner Metabolic networks and their evolution. , 2012, Advances in experimental medicine and biology.

[11]  H. Nelis,et al.  Isolation and identification of quorum quenching bacteria from environmental samples. , 2011, Journal of microbiological methods.

[12]  D. Jendrossek,et al.  Identification of a multifunctional protein, PhaM, that determines number, surface to volume ratio, subcellular localization and distribution to daughter cells of poly(3‐hydroxybutyrate), PHB, granules in Ralstonia eutropha H16 , 2011, Molecular microbiology.

[13]  D. Jendrossek,et al.  Interaction between poly(3-hydroxybutyrate) granule-associated proteins as revealed by two-hybrid analysis and identification of a new phasin in Ralstonia eutropha H16. , 2011, Microbiology.

[14]  S. D. Das Gupta,et al.  Whole-Genome Shotgun Sequencing of the Sulfur-Oxidizing Chemoautotroph Tetrathiobacter kashmirensis , 2011, Journal of bacteriology.

[15]  R. Sinha,et al.  Rhizosphere of rice plants harbor bacteria with multiple plant growth promoting features , 2011 .

[16]  M. S. Reddy,et al.  Genetic Diversity and Phylogeny of Antagonistic Bacteria against Phytophthora nicotianae Isolated from Tobacco Rhizosphere , 2011, International journal of molecular sciences.

[17]  A. Steinbüchel,et al.  Novel Reaction of Succinyl Coenzyme A (Succinyl-CoA) Synthetase: Activation of 3-Sulfinopropionate to 3-Sulfinopropionyl-CoA in Advenella mimigardefordensis Strain DPN7T during Degradation of 3,3′-Dithiodipropionic Acid , 2011, Journal of bacteriology.

[18]  A. Filloux,et al.  Type VI Secretion System in Pseudomonas aeruginosa , 2011, The Journal of Biological Chemistry.

[19]  H. Riveros-Rosas,et al.  Bacterial transport of sulfate, molybdate, and related oxyanions , 2011, BioMetals.

[20]  A. Steinbüchel,et al.  Dihydrolipoamide Dehydrogenases of Advenella mimigardefordensis and Ralstonia eutropha Catalyze Cleavage of 3,3′-Dithiodipropionic Acid into 3-Mercaptopropionic Acid , 2010, Applied and Environmental Microbiology.

[21]  P. Cotter,et al.  Type VI secretion: not just for pathogenesis anymore. , 2010, Cell host & microbe.

[22]  D. Goodlett,et al.  A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. , 2010, Cell host & microbe.

[23]  S. Amalfitano,et al.  The role of a groundwater bacterial community in the degradation of the herbicide terbuthylazine. , 2010, FEMS microbiology ecology.

[24]  D. DeShazer,et al.  Burkholderia mallei Cluster 1 Type VI Secretion Mutants Exhibit Growth and Actin Polymerization Defects in RAW 264.7 Murine Macrophages , 2009, Infection and Immunity.

[25]  P. Grenni,et al.  Reclassification of the members of the genus Tetrathiobacter Ghosh et al. 2005 to the genus Advenella Coenye et al. 2005. , 2009, International journal of systematic and evolutionary microbiology.

[26]  B. Dam,et al.  Conjugative Type 4 Secretion System of a Novel Large Plasmid from the Chemoautotroph Tetrathiobacter kashmirensis and Construction of Shuttle Vectors for Alcaligenaceae , 2009, Applied and Environmental Microbiology.

[27]  Michel Hébraud,et al.  Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. , 2009, Trends in microbiology.

[28]  D. Espinosa-Victoria,et al.  USE OF 16S rRNA GENE FOR CHARACTERIZATION OF PHOSPHATE-SOLUBILIZING BACTERIA ASSOCIATED WITH CORN USO DEL GEN 16S rRNA PARA CARACTERIZACIÓN DE BACTERIAS SOLUBILIZADORAS DE FOSFATOS ASOCIADAS AL MAÍZ , 2009 .

[29]  A. Steinbüchel,et al.  3-Mercaptopropionate Dioxygenase, a Cysteine Dioxygenase Homologue, Catalyzes the Initial Step of 3-Mercaptopropionate Catabolism in the 3,3-Thiodipropionic Acid-degrading Bacterium Variovorax paradoxus* , 2009, Journal of Biological Chemistry.

[30]  B. Eikmanns,et al.  Identification and Characterization of a Bacterial Transport System for the Uptake of Pyruvate, Propionate, and Acetate in Corynebacterium glutamicum , 2008, Journal of bacteriology.

[31]  Charles Elkan,et al.  The Transporter Classification Database: recent advances , 2008, Nucleic Acids Res..

[32]  James R. Cole,et al.  The Ribosomal Database Project: improved alignments and new tools for rRNA analysis , 2008, Nucleic Acids Res..

[33]  Kazuya Watanabe,et al.  Phylogenetic analyses of bacterial communities developed in a cassette-electrode microbial fuel cell. , 2009, Microbes and environments.

[34]  J. Contiero,et al.  Glycerol: a promising and abundant carbon source for industrial microbiology. , 2009, Biotechnology advances.

[35]  K. Jahreis,et al.  Ins and outs of glucose transport systems in eubacteria. , 2008, FEMS microbiology reviews.

[36]  A. Steinbüchel,et al.  Ralstonia eutropha Strain H16 as Model Organism for PHA Metabolism and for Biotechnological Production of Technically Interesting Biopolymers , 2008, Journal of Molecular Microbiology and Biotechnology.

[37]  B. Singh,et al.  The role of Variovorax and other Comamonadaceae in sulfur transformations by microbial wheat rhizosphere communities exposed to different sulfur fertilization regimes. , 2008, Environmental microbiology.

[38]  A. Steinbüchel,et al.  Novel Pathway for Catabolism of the Organic Sulfur Compound 3,3′-Dithiodipropionic Acid via 3-Mercaptopropionic Acid and 3-Sulfinopropionic Acid to Propionyl-Coenzyme A by the Aerobic Bacterium Tetrathiobacter mimigardefordensis Strain DPN7 , 2008, Applied and Environmental Microbiology.

[39]  D. Manter,et al.  Bio-Reduction of Selenite to Elemental Red Selenium by Tetrathiobacter kashmirensis , 2008, Current Microbiology.

[40]  F. Spinozzi,et al.  Binding of the Major Phasin, PhaP1, from Ralstonia eutropha H16 to Poly(3-Hydroxybutyrate) Granules , 2008, Journal of bacteriology.

[41]  U. Kappler Bacterial Sulfite-Oxidizing Enzymes – Enzymes for Chemolithotrophs Only? , 2008 .

[42]  M. Moran,et al.  Transcriptional response of Silicibacter pomeroyi DSS-3 to dimethylsulfoniopropionate (DMSP). , 2007, Environmental microbiology.

[43]  K. Schleifer,et al.  Characterization of bacterial operons consisting of two tubulins and a kinesin-like gene by the novel Two-Step Gene Walking method , 2007, Nucleic Acids Research.

[44]  S. Sievert,et al.  The sulfur cycle , 2007 .

[45]  Sukhendu Mandal,et al.  The S4-intermediate pathway for the oxidation of thiosulfate by the chemolithoautotroph Tetrathiobacter kashmirensis and inhibition of tetrathionate oxidation by sulfite. , 2007, Research in microbiology.

[46]  Susanne Rath,et al.  Electrochemical behavior of dopamine at a 3,3'-dithiodipropionic acid self-assembled monolayers. , 2007, Talanta.

[47]  H. Kricheldorf,et al.  Poly(thioester)s , 2007 .

[48]  M. Steinke,et al.  Structural and Regulatory Genes Required to Make the Gas Dimethyl Sulfide in Bacteria , 2007, Science.

[49]  A. Schmalenberger,et al.  Desulfurization of aromatic sulfonates by rhizosphere bacteria: high diversity of the asfA gene. , 2007, Environmental microbiology.

[50]  C. Locht,et al.  Structural analysis of Bordetella pertussis BugE solute receptor in a bound conformation. , 2006, Acta crystallographica. Section D, Biological crystallography.

[51]  Anne Pohlmann,et al.  Genome sequence of the bioplastic-producing “Knallgas” bacterium Ralstonia eutropha H16 , 2006, Nature Biotechnology.

[52]  P. Vandamme,et al.  Tetrathiobacter mimigardefordensis sp. nov., isolated from compost, a betaproteobacterium capable of utilizing the organic disulfide 3,3'-dithiodipropionic acid. , 2006, International journal of systematic and evolutionary microbiology.

[53]  P. Vandamme,et al.  Growth in Stewart's medium is a simple, rapid and inexpensive screening tool for the identification of Burkholderia cepacia complex. , 2006, Journal of cystic fibrosis : official journal of the European Cystic Fibrosis Society.

[54]  W. Nelson,et al.  Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[55]  A. M. Cook,et al.  Dissimilation of C 3 -sulfonates , 2006 .

[56]  A. M. Cook,et al.  Dissimilation of C3-sulfonates , 2006, Archives of Microbiology.

[57]  Alexander Steinbüchel,et al.  Non-biodegradable biopolymers from renewable resources: perspectives and impacts. , 2005, Current opinion in biotechnology.

[58]  J. Foght,et al.  Bacterial biodegradation of aliphatic sulfides under aerobic carbon‐ or sulfur‐limited growth conditions , 2005, Journal of applied microbiology.

[59]  R. Wogelius,et al.  Importance of Organosulfur Utilization for Survival of Pseudomonas putida in Soil and Rhizosphere , 2005, Applied and Environmental Microbiology.

[60]  Angshuman Bagchi,et al.  Tetrathiobacter kashmirensis gen. nov., sp. nov., a novel mesophilic, neutrophilic, tetrathionate-oxidizing, facultatively chemolithotrophic betaproteobacterium isolated from soil from a temperate orchard in Jammu and Kashmir, India. , 2005, International journal of systematic and evolutionary microbiology.

[61]  C. Locht,et al.  The periplasmic binding protein of a tripartite tricarboxylate transporter is involved in signal transduction. , 2005, Journal of molecular biology.

[62]  Søren Brunak,et al.  Prediction of twin-arginine signal peptides , 2005, BMC Bioinformatics.

[63]  F. Heffron,et al.  sciS, an icmF Homolog in Salmonella enterica Serovar Typhimurium, Limits Intracellular Replication and Decreases Virulence , 2005, Infection and Immunity.

[64]  C. Friedrich,et al.  Prokaryotic sulfur oxidation. , 2005, Current opinion in microbiology.

[65]  R. Gueta,et al.  Dissimilation of cysteate via 3-sulfolactate sulfo-lyase and a sulfate exporter in Paracoccus pantotrophus NKNCYSA. , 2005, Microbiology.

[66]  J. Honek,et al.  Biological chemistry of naturally occurring thiols of microbial and marine origin. , 2005, Journal of natural products.

[67]  A. Steinbüchel,et al.  Poly(3-mercaptopropionate): a nonbiodegradable biopolymer? , 2005, Biomacromolecules.

[68]  A. Steinbüchel,et al.  Poly(3-hydroxybutyrate) granule-associated proteins: impacts on poly(3-hydroxybutyrate) synthesis and degradation. , 2005, Biomacromolecules.

[69]  P. Vandamme,et al.  Advenella incenata gen. nov., sp. nov., a novel member of the Alcaligenaceae, isolated from various clinical samples. , 2005, International journal of systematic and evolutionary microbiology.

[70]  T. Lütke-Eversloh,et al.  Studies on the biodegradability of polythioester copolymers and homopolymers by polyhydroxyalkanoate (PHA)-degrading bacteria and PHA depolymerases , 2004, Archives of Microbiology.

[71]  M. Kertesz,et al.  The role of soil microbes in plant sulphur nutrition. , 2004, Journal of experimental botany.

[72]  A. M. Cook,et al.  Enzymes and genes of taurine and isethionate dissimilation in Paracoccus denitrificans. , 2004, Microbiology.

[73]  Tan Ikp Polyhydroxyalkanoate production from renewable resources , 2004 .

[74]  H. Schlegel,et al.  Ein Submersverfahren zur Kultur wasserstoffoxydierender Bakterien: Wachstumsphysiologische Untersuchungen , 2004, Archiv für Mikrobiologie.

[75]  A. Steinbüchel,et al.  Microbial polythioesters. , 2004, Macromolecular bioscience.

[76]  R. Simon High frequency mobilization of gram-negative bacterial replicons by the in vitro constructed Tn5-Mob transposon , 2004, Molecular and General Genetics MGG.

[77]  A. Steinbüchel,et al.  Physical properties of microbial polythioesters: characterization of poly(3-mercaptoalkanoates) synthesized by engineered Escherichia coli. , 2003, Biomacromolecules.

[78]  P. Bork,et al.  Metabolites: a helping hand for pathway evolution? , 2003, Trends in biochemical sciences.

[79]  A. Steinbüchel,et al.  Novel precursor substrates for polythioesters (PTE) and limits of PTE biosynthesis in Ralstonia eutropha. , 2003, FEMS microbiology letters.

[80]  E. Willery,et al.  Overrepresentation of a Gene Family Encoding Extracytoplasmic Solute Receptors in Bordetella , 2003, Journal of bacteriology.

[81]  Natalia Ivanova,et al.  The ERGOTM genome analysis and discovery system , 2003, Nucleic Acids Res..

[82]  Rainer Merkl,et al.  YACOP: Enhanced gene prediction obtained by a combination of existing methods , 2003, Silico Biol..

[83]  Hellmut Eckert,et al.  Biosynthesis of novel thermoplastic polythioesters by engineered Escherichia coli , 2002, Nature materials.

[84]  D. C. Yoch Dimethylsulfoniopropionate: Its Sources, Role in the Marine Food Web, and Biological Degradation to Dimethylsulfide , 2002, Applied and Environmental Microbiology.

[85]  A. M. Cook,et al.  Dissimilation of the C2 sulfonates , 2002, Archives of Microbiology.

[86]  A. Steinbüchel,et al.  Characterization of microbial polythioesters: physical properties of novel copolymers synthesized by Ralstonia eutropha. , 2002, Biomacromolecules.

[87]  Vincent Lombard,et al.  The EMBL Nucleotide Sequence Database , 2002, Nucleic Acids Res..

[88]  Zhengxiang Wang,et al.  Glycerol production by microbial fermentation: a review. , 2001, Biotechnology advances.

[89]  C. M. G. van den Berg,et al.  Thiols in coastal waters of the western North Sea and English Channel. , 2001, Environmental science & technology.

[90]  A. Steinbüchel,et al.  Identification of a new class of biopolymer: bacterial synthesis of a sulfur-containing polymer with thioester linkages. , 2001, Microbiology.

[91]  T. Endo,et al.  Cationic ring-opening polymerization of ∊-thionocaprolactone: Selective formation of polythioester , 2000 .

[92]  Kim Rutherford,et al.  Artemis: sequence visualization and annotation , 2000, Bioinform..

[93]  S. Copley,et al.  Evolution of a metabolic pathway for degradation of a toxic xenobiotic: the patchwork approach. , 2000, Trends in biochemical sciences.

[94]  T. Leisinger,et al.  Deletion Analysis of the Escherichia coli Taurine and Alkanesulfonate Transport Systems , 2000, Journal of bacteriology.

[95]  M. Kertesz Riding the sulfur cycle--metabolism of sulfonates and sulfate esters in gram-negative bacteria. , 2000, FEMS microbiology reviews.

[96]  T. Leustek,et al.  Identification of a New Class of 5′-Adenylylsulfate (APS) Reductases from Sulfate-Assimilating Bacteria , 2000, Journal of bacteriology.

[97]  Kathryn F. Beal,et al.  The Staden package, 1998. , 2000, Methods in molecular biology.

[98]  H. Tsutsumi,et al.  A potentially biodegradable polyamide containing disulfide bonds as a positive material for secondary batteries , 1998 .

[99]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[100]  Ploeg,et al.  Identification of sulfate starvation-regulated genes in Escherichia coli: a gene cluster involved in the utilization of taurine as a sulfur source , 1996, Journal of bacteriology.

[101]  E. Getzoff,et al.  Sulfite Reductase Structure at 1.6 Å: Evolution and Catalysis for Reduction of Inorganic Anions , 1995, Science.

[102]  T. Conway,et al.  The Entner-Doudoroff pathway: history, physiology and molecular biology. , 1992, FEMS microbiology reviews.

[103]  B. F. Taylor,et al.  Biotransformations of organosulphur compounds in sediments via 3-mercaptopropionate , 1988, Nature.

[104]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[105]  F. Neidhardt,et al.  Linkage Map of Escherichia coli K-12 , 1987 .

[106]  A. H. Romano Microbial sugar transport systems and their importance in biotechnology , 1986 .

[107]  K. Kersters,et al.  Intra- and intergeneric similarities of the Bordetella ribosomal ribonucleic acid cistrons: proposal for a new family, Alcaligenaceae , 1986 .

[108]  Alka Gupta,et al.  Electrochemical studies on the composition, stability constants and thermodynamics of TI(I) complexes with dithiodipropionic acid , 1984 .

[109]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[110]  A. Pühler,et al.  A Broad Host Range Mobilization System for In Vivo Genetic Engineering: Transposon Mutagenesis in Gram Negative Bacteria , 1983, Bio/Technology.

[111]  B. Friedrich,et al.  Naturally occurring genetic transfer of hydrogen-oxidizing ability between strains of Alcaligenes eutrophus , 1981, Journal of bacteriology.

[112]  A. Gunnison Sulphite toxicity: a critical review of in vitro and in vivo data. , 1981, Food and cosmetics toxicology.

[113]  E. C. Lin,et al.  Glycerol dissimilation and its regulation in bacteria. , 1976, Annual review of microbiology.

[114]  B. Jollés-Bergeret Enzymatic and chemical synthesis of 3-sulfinopropionic acid, an analog of succinic acid. , 1974, European journal of biochemistry.

[115]  M. Ishimoto,et al.  Enzymatic formation of sulfite and acetate from sulfoacetaldehyde, a degradation product of taurine. , 1972, Journal of biochemistry.

[116]  G. Gottschalk,et al.  [A submersion method for culture of hydrogen-oxidizing bacteria: growth physiological studies]. , 1961, Archiv fur Mikrobiologie.

[117]  J. L. Bailey,et al.  Studies on the reaction of sulfite with proteins. , 1959, The Journal of biological chemistry.