1887

Abstract

Bioremediation of metaldehyde from drinking water using metaldehyde-degrading strains has recently emerged as a promising alternative. Whole-genome sequencing was used to obtain full genomes for metaldehyde degraders E1 and CMET-H. For the former, the genetic context of the metaldehyde-degrading genes had not been explored, while for the latter, none of the degrading genes themselves had been identified. In E1, IS and IS-family insertion sequences (ISs) were found surrounding the metaldehyde-degrading gene cluster located in plasmid pAME76. This cluster was located in closely-related plasmids and associated to identical ISs in most metaldehyde-degrading β- and γ-Proteobacteria, indicating horizontal gene transfer (HGT). For CMET-H, sequence analysis suggested a phytanoyl-CoA family oxygenase as a metaldehyde-degrading gene candidate due to its close homology to a previously identified metaldehyde-degrading gene known as . Heterologous gene expression in alongside degradation tests verified its functional significance and the degrading gene homolog was henceforth called . It was found that is hosted within the conjugative plasmid pSM1 and its genetic context suggested a crossover between the metaldehyde and acetoin degradation pathways. Here, specific replicons and ISs responsible for maintaining and dispersing metaldehyde-degrading genes in α, β and γ-Proteobacteria through HGT were identified and described. In addition, a homologous gene implicated in the first step of metaldehyde utilisation in an α-Proteobacteria was uncovered. Insights into specific steps of this possible degradation pathway are provided.

Funding
This study was supported by the:
  • Universidad de Costa Rica
    • Principle Award Recipient: VíctorCastro-Gutierrez
  • Ministerio de Educación y Formación Profesional (Award PID2020-117923GB-I00)
    • Principle Award Recipient: MaríaPilar Garcillán-Barcia
  • Natural Environment Research Council (Award NE/N009061/1)
    • Principle Award Recipient: JamesMoir
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2022-10-27
2024-12-05
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References

  1. Cooke A, Rettino J, Flower L, Filby K, Freer A. Farming for water; catchment management initiatives for reducing pesticides. Water Environ J 2020; 34:679–691 [View Article]
    [Google Scholar]
  2. Cosgrove S, Jefferson B, Jarvis P. Pesticide removal from drinking water sources by adsorption: a review. Environ Technol Rev 2019; 8:1–24 [View Article]
    [Google Scholar]
  3. Dillon G, Hall T, Jönsson J, Rockett L, Shepherd D et al. Emerging pesticides; what next. Report Ref No 13/DW/14/6 2013
    [Google Scholar]
  4. Leahy JG, Colwell RR. Microbial degradation of hydrocarbons in the environment. Microbiol Rev 1990; 54:305–315 [View Article] [PubMed]
    [Google Scholar]
  5. Castro-Gutierrez VM, Pickering L, Cambronero-Heinrichs JC, Holden B, Haley J et al. Bioaugmentation of pilot-scale slow sand filters can achieve compliant levels for the micropollutant metaldehyde in a real water matrix. Water Res 2022; 211:118071 [View Article] [PubMed]
    [Google Scholar]
  6. Thomas JC, Helgason T, Sinclair CJ, Moir JWB. Isolation and characterization of metaldehyde-degrading bacteria from domestic soils. Microb Biotechnol 2017; 10:1824–1829 [View Article] [PubMed]
    [Google Scholar]
  7. Castro-Gutiérrez V, Fuller E, Thomas JC, Sinclair CJ, Johnson S et al. Genomic basis for pesticide degradation revealed by selection, isolation and characterisation of a library of metaldehyde-degrading strains from soil. Soil Biol Biochem 2020; 142:107702 [View Article]
    [Google Scholar]
  8. Castro-Gutierrez VM, Hassard F, Moir JWB. Probe-based qPCR assay enables the rapid and specific detection of bacterial degrading genes for the pesticide metaldehyde in soil. J Microbiol Methods 2022; 195:106447 [View Article]
    [Google Scholar]
  9. Partridge SR, Kwong SM, Firth N, Jensen SO. Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev 2018; 31:e00088-17 [View Article]
    [Google Scholar]
  10. Rios Miguel AB, Jetten MSM, Welte CU. The role of mobile genetic elements in organic micropollutant degradation during biological wastewater treatment. Water Res X 2020; 9:100065 [View Article]
    [Google Scholar]
  11. Franklin FCH, Bagdasarian M, Bagdasarian MM, Timmis KN. Molecular and functional analysis of the TOL plasmid pWWO from Pseudomonas putida and cloning of genes for the entire regulated aromatic ring meta cleavage pathway. Proc Natl Acad Sci U S A 1981; 78:7458–7462 [View Article] [PubMed]
    [Google Scholar]
  12. Mulbry WW, Karns JS, Kearney PC, Nelson JO, McDaniel CS et al. Identification of a plasmid-borne parathion hydrolase gene from Flavobacterium sp. by southern hybridization with opd from Pseudomonas diminuta. Appl Environ Microbiol 1986; 51:926–930 [View Article] [PubMed]
    [Google Scholar]
  13. Siddavattam D, Khajamohiddin S, Manavathi B, Pakala SB, Merrick M. Transposon-like organization of the plasmid-borne organophosphate degradation (opd) gene cluster found in Flavobacterium sp. Appl Environ Microbiol 2003; 69:2533–2539 [View Article] [PubMed]
    [Google Scholar]
  14. Gallego S, Devers-Lamrani M, Rousidou K, Karpouzas DG, Martin-Laurent F. Assessment of the effects of oxamyl on the bacterial community of an agricultural soil exhibiting enhanced biodegradation. Sci Total Environ 2019; 651:1189–1198 [View Article] [PubMed]
    [Google Scholar]
  15. Devers M, El Azhari N, Kolic N-U, Martin-Laurent F. Detection and organization of atrazine-degrading genetic potential of seventeen bacterial isolates belonging to divergent taxa indicate a recent common origin of their catabolic functions. FEMS Microbiol Lett 2007; 273:78–86 [View Article] [PubMed]
    [Google Scholar]
  16. Öztürk B, Werner J, Meier-Kolthoff JP, Bunk B, Spröer C et al. Comparative genomics suggests mechanisms of genetic adaptation toward the catabolism of the phenylurea herbicide linuron in variovorax. Genome Biol Evol 2020; 12:827–841 [View Article] [PubMed]
    [Google Scholar]
  17. Lopez-Echartea E, Suman J, Smrhova T, Ridl J, Pajer P et al. Genomic analysis of dibenzofuran-degrading Pseudomonas veronii strain Pvy reveals its biodegradative versatility. G3 Genes 2021; 11:jkaa030 [View Article]
    [Google Scholar]
  18. Nielsen TK, Horemans B, Lood C, T’Syen J, van Noort V et al. The complete genome of 2,6-dichlorobenzamide (BAM) degrader Aminobacter sp. MSH1 suggests a polyploid chromosome, phylogenetic reassignment, and functions of plasmids. Sci Rep 2021; 11:111 [View Article]
    [Google Scholar]
  19. Azam S, Parthasarathy S, Singh C, Kumar S, Siddavattam D. Genome organization and adaptive potential of archetypal organophosphate degrading sphingobium fuliginis ATCC 27551. Genome Biol Evol 2019; 11:2557–2562 [View Article] [PubMed]
    [Google Scholar]
  20. Ikuma K, Gunsch CK. Genetic bioaugmentation as an effective method for in situ bioremediation: functionality of catabolic plasmids following conjugal transfers. Bioengineered 2012; 3:236–241 [View Article]
    [Google Scholar]
  21. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  22. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLOS Comput Biol 2017; 13:e1005595 [View Article]
    [Google Scholar]
  23. Wick RR, Schultz MB, Zobel J, Holt KE. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 2015; 31:3350–3352 [View Article] [PubMed]
    [Google Scholar]
  24. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  25. Antipov D, Hartwick N, Shen M, Raiko M, Lapidus A et al. PlasmidSPAdes: assembling plasmids from whole genome sequencing data. Bioinformatics 2016; 32:3380–3387 [View Article] [PubMed]
    [Google Scholar]
  26. Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ et al. Fast genome-wide functional annotation through orthology Assignment by eggNOG-mapper. Mol Biol Evol 2017; 34:2115–2122 [View Article] [PubMed]
    [Google Scholar]
  27. Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 2019; 47:D309–D314 [View Article] [PubMed]
    [Google Scholar]
  28. Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T et al. Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 2017; 45:D535–D542 [View Article] [PubMed]
    [Google Scholar]
  29. Luo H, Gao F. DoriC 10.0: an updated database of replication origins in prokaryotic genomes including chromosomes and plasmids. Nucleic Acids Res 2019; 47:D74–D77 [View Article] [PubMed]
    [Google Scholar]
  30. Carver T, Harris SR, Berriman M, Parkhill J, McQuillan JA. Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 2012; 28:464–469 [View Article] [PubMed]
    [Google Scholar]
  31. Lagesen K, Hallin P, Rødland EA, Staerfeldt H-H, Rognes T et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100–3108 [View Article] [PubMed]
    [Google Scholar]
  32. Lowe TM, Chan PP. tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 2016; 44:W54–7 [View Article]
    [Google Scholar]
  33. Li X, Xie Y, Liu M, Tai C, Sun J et al. oriTfinder: a web-based tool for the identification of origin of transfers in DNA sequences of bacterial mobile genetic elements. Nucleic Acids Res 2018; 46:W229–W234 [View Article] [PubMed]
    [Google Scholar]
  34. Garcillán-Barcia MP, Redondo-Salvo S, Vielva L, de la Cruz F. MOBscan: automated annotation of MOB relaxases. Methods Mol Biol 2020; 2075:295–308 [View Article] [PubMed]
    [Google Scholar]
  35. Abby SS, Néron B, Ménager H, Touchon M, Rocha EPC. MacSyFinder: a program to mine genomes for molecular systems with an application to CRISPR-Cas systems. PLoS One 2014; 9:e110726 [View Article]
    [Google Scholar]
  36. Redondo-Salvo S, Bartomeus-Peñalver R, Vielva L, Tagg KA, Webb HE et al. COPLA, a taxonomic classifier of plasmids. BMC Bioinformatics 2021; 22:390 [View Article]
    [Google Scholar]
  37. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 2006; 34:D32–6 [View Article]
    [Google Scholar]
  38. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A et al. InterPro: the integrative protein signature database. Nucleic Acids Res 2009; 37:D211–5 [View Article]
    [Google Scholar]
  39. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  40. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 2009; 25:119–120 [View Article] [PubMed]
    [Google Scholar]
  41. Roosaare M, Puustusmaa M, Möls M, Vaher M, Remm M. PlasmidSeeker: identification of known plasmids from bacterial whole genome sequencing reads. PeerJ 2018; 6:e4588 [View Article] [PubMed]
    [Google Scholar]
  42. Gertz EM, Yu Y-K, Agarwala R, Schäffer AA, Altschul SF. Composition-based statistics and translated nucleotide searches: improving the TBLASTN module of BLAST. BMC Biol 2006; 4:41 [View Article] [PubMed]
    [Google Scholar]
  43. Fuller E. Identification and Characterization of the Biological Mechanisms of Metaldehyde Degradation University of York; 2021
    [Google Scholar]
  44. Potter SC, Luciani A, Eddy SR, Park Y, Lopez R et al. HMMER web server: 2018 update. Nucleic Acids Res 2018; 46:W200–W204 [View Article] [PubMed]
    [Google Scholar]
  45. Eddy SR. A new generation of homology search tools based on probabilistic inference. Genome Inform 2009; 23:205–211
    [Google Scholar]
  46. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast fourier transform. Nucleic Acids Res 2002; 30:3059–3066 [View Article] [PubMed]
    [Google Scholar]
  47. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article] [PubMed]
    [Google Scholar]
  48. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 2017; 14:587–589 [View Article] [PubMed]
    [Google Scholar]
  49. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  50. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 2018; 35:518–522 [View Article] [PubMed]
    [Google Scholar]
  51. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
    [Google Scholar]
  52. Fogg MJ, Wilkinson AJ. Higher-throughput approaches to crystallization and crystal structure determination. Biochem Soc Trans 2008; 36:771–775 [View Article] [PubMed]
    [Google Scholar]
  53. Cold Spring Harbor Sds-Page gel. Cold Spring Harb Protoc 2015; 2015:pdb.rec087908
    [Google Scholar]
  54. Tao B, Fletcher AJ. Metaldehyde removal from aqueous solution by adsorption and ion exchange mechanisms onto activated carbon and polymeric sorbents. J Hazard Mater 2013; 244–245:240–250 [View Article] [PubMed]
    [Google Scholar]
  55. Mammeri H, Poirel L, Mangeney N, Nordmann P. Chromosomal integration of a cephalosporinase gene from Acinetobacter baumannii into Oligella urethralis as a source of acquired resistance to beta-lactams. Antimicrob Agents Chemother 2003; 47:1536–1542 [View Article] [PubMed]
    [Google Scholar]
  56. Ravenhall M, Škunca N, Lassalle F, Dessimoz C. Inferring horizontal gene transfer. PLoS Comput Biol 2015; 11:1–16 [View Article] [PubMed]
    [Google Scholar]
  57. Collier LS, Gaines GL, Neidle EL. Regulation of benzoate degradation in Acinetobacter sp. strain ADP1 by BenM, a LysR-type transcriptional activator. J Bacteriol 1998; 180:2493–2501 [View Article] [PubMed]
    [Google Scholar]
  58. Mindlin S, Petrenko A, Kurakov A, Beletsky A, Mardanov A et al. Resistance of permafrost and modern Acinetobacter lwoffii strains to heavy metals and arsenic revealed by genome analysis. Biomed Res Int 2016; 2016:3970831 [View Article] [PubMed]
    [Google Scholar]
  59. Providenti MA, O’Brien JM, Ewing RJ, Paterson ES, Smith ML. The copy-number of plasmids and other genetic elements can be determined by SYBR-Green-based quantitative real-time PCR. J Microbiol Methods 2006; 65:476–487 [View Article] [PubMed]
    [Google Scholar]
  60. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  61. Clarke TE, Romanov V, Chirgadze YN, Klomsiri C, Kisselman G et al. Crystal structure of alkyl hydroperoxidase D like protein PA0269 from Pseudomonas aeruginosa: Homology of the AhpD-like structural family. BMC Struct Biol 2011; 11:1–12 [View Article]
    [Google Scholar]
  62. Huang M, Oppermann-Sanio FB, Steinbüchel A. Biochemical and molecular characterization of the Bacillus subtilis acetoin catabolic pathway. J Bacteriol 1999; 181:3837–3841 [View Article] [PubMed]
    [Google Scholar]
  63. Xiao ZJ, Huang YL, Zhu XK, Qiao SL. Functional study of AcoX, an unknown protein involved in acetoin catabolism. AMR 2012; 393–395:776–779 [View Article]
    [Google Scholar]
  64. Nojiri H, Shintani M, Omori T. Divergence of mobile genetic elements involved in the distribution of xenobiotic-catabolic capacity. Appl Microbiol Biotechnol 2004; 64:154–174 [View Article] [PubMed]
    [Google Scholar]
  65. Cabezón E, Ripoll-Rozada J, Peña A, de la Cruz F, Arechaga I. Towards an integrated model of bacterial conjugation. FEMS Microbiol Rev 2015; 39:81–95 [View Article] [PubMed]
    [Google Scholar]
  66. Smillie C, Garcillán-Barcia MP, Francia MV, Rocha EPC, de la Cruz F. Mobility of plasmids. Microbiol Mol Biol Rev 2010; 74:434–452 [View Article] [PubMed]
    [Google Scholar]
  67. Jung J, Park W. Acinetobacter species as model microorganisms in environmental microbiology: current state and perspectives. Appl Microbiol Biotechnol 2015; 99:2533–2548 [View Article] [PubMed]
    [Google Scholar]
  68. Palmen R, Hellingwerf KJ. Uptake and processing of DNA by Acinetobacter calcoaceticus--a review. Gene 1997; 192:179–190 [View Article] [PubMed]
    [Google Scholar]
  69. Melnikov A, Youngman PJ. Random mutagenesis by recombinational capture of PCR products in Bacillus subtilis and Acinetobacter calcoaceticus. Nucleic Acids Res 1999; 27:1056–1062 [View Article] [PubMed]
    [Google Scholar]
  70. Wyndham RC, Cashore AE, Nakatsu CH, Peel MC. Catabolic transposons. Biodegradation 1994; 5:323–342 [View Article] [PubMed]
    [Google Scholar]
  71. Springael D, van Thor J, Goorissen H, Ryngaert A, De Baere R et al. RP4::Mu3A-mediated in vivo cloning and transfer of a chlorobiphenyl catabolic pathway. Microbiology 1996; 142:3283–3293 [View Article]
    [Google Scholar]
  72. Varani A, He S, Siguier P, Ross K, Chandler M. The IS6 family, a clinically important group of insertion sequences including IS26. Mob DNA 2021; 12:1–18 [View Article] [PubMed]
    [Google Scholar]
  73. Harmer CJ, Hall RM. An analysis of the IS6/IS26 family of insertion sequences: is it a single family?. Microb Genom 2019; 5: [View Article]
    [Google Scholar]
  74. Blackwell GA, Nigro SJ, Hall RM. Evolution of AbGRI2-0, the progenitor of the AbGRI2 resistance island in global Clone 2 of Acinetobacter baumannii. Antimicrob Agents Chemother 2015; 60:1421–1429 [View Article] [PubMed]
    [Google Scholar]
  75. Post V, Hall RM. AbaR5, a large multiple-antibiotic resistance region found in Acinetobacter baumannii. Antimicrob Agents Chemother 2009; 53:2667–2671 [View Article] [PubMed]
    [Google Scholar]
  76. Mollet B, Iida S, Arber W. Gene organization and target specificity of the prokaryotic mobile genetic element IS26. Mol Gen Genet 1985; 201:198–203 [View Article] [PubMed]
    [Google Scholar]
  77. Harmer CJ, Hall RM. IS 26 family members IS 257 and IS 1216 also form cointegrates by copy-in and targeted conservative routes. mSphere 2020 [View Article]
    [Google Scholar]
  78. Harmer CJ, Moran RA, Hall RM. Movement of IS26-associated antibiotic resistance genes occurs via a translocatable unit that includes a single IS26 and preferentially inserts adjacent to another IS26. mBio 2014; 5:e01801–14 [View Article] [PubMed]
    [Google Scholar]
  79. Mollet B, Iida S, Shepherd J, Arber W. Nucleotide sequence of IS26, a new prokaryotic mobile genetic element. Nucleic Acids Res 1983; 11:6319–6330 [View Article] [PubMed]
    [Google Scholar]
  80. Iida S, Mollet B, Meyer J, Arber W. Functional characterization of the prokaryotic mobile genetic element IS26. Mol Gen Genet 1984; 198:84–89 [View Article]
    [Google Scholar]
  81. Harmer CJ, Hall RM. IS26-mediated formation of transposons carrying antibiotic resistance genes. mSphere 2016; 1:e00038-16 [View Article]
    [Google Scholar]
  82. Kholodii G, Mindlin S, Gorlenko Z, Petrova M, Hobman J et al. Translocation of transposition-deficient (TndPKLH2-like) transposons in the natural environment: mechanistic insights from the study of adjacent DNA sequences. Microbiology 2004; 150:979–992 [View Article]
    [Google Scholar]
  83. Garcillán-Barcia MP, de la Cruz F. Distribution of IS91 family insertion sequences in bacterial genomes: evolutionary implications. FEMS Microbiol Ecol 2002; 42:303–313 [View Article] [PubMed]
    [Google Scholar]
  84. Mahillon J, Chandler M. Insertion sequences. Microbiol Mol Biol Rev 1998; 62:725–774 [View Article] [PubMed]
    [Google Scholar]
  85. del Pilar Garcillán-Barcia M, Bernales I, Mendiola MV, de la Cruz F. Single-stranded DNA intermediates in IS91 rolling-circle transposition. Mol Microbiol 2001; 39:494–501 [View Article]
    [Google Scholar]
  86. Garcillán-Barcia M, Bernales I, Mendiola MV, La CF. IS91 Rolling-Circle Transposition. In Craig N. eds Mobile DNA II Washington D.C: American Society of Microbiology; 2002 pp 891–904
    [Google Scholar]
  87. Tavakoli N, Comanducci A, Dodd HM, Lett MC, Albiger B et al. IS1294, a DNA element that transposes by RC transposition. Plasmid 2000; 44:66–84 [View Article] [PubMed]
    [Google Scholar]
  88. Mendiola MV, Bernales I, de la Cruz F. Differential roles of the transposon termini in IS91 transposition. Proc Natl Acad Sci U S A 1994; 91:1922–1926 [View Article] [PubMed]
    [Google Scholar]
  89. Diaz-Aroca E, Mendiola MV, Zabala JC, de la Cruz F. Transposition of IS91 does not generate a target duplication. J Bacteriol 1987; 169:442–443 [View Article] [PubMed]
    [Google Scholar]
  90. Xiao Z, Xu P. Acetoin metabolism in bacteria. Crit Rev Microbiol 2007; 33:127–140 [View Article]
    [Google Scholar]
  91. Oppermann FB, Schmidt B, Steinbüchel A. Purification and characterization of acetoin:2,6-dichlorophenolindophenol oxidoreductase, dihydrolipoamide dehydrogenase, and dihydrolipoamide acetyltransferase of the Pelobacter carbinolicus acetoin dehydrogenase enzyme system. J Bacteriol 1991; 173:757–767 [View Article] [PubMed]
    [Google Scholar]
  92. Dauner M, Sonderegger M, Hochuli M, Szyperski T, Wüthrich K et al. Intracellular carbon fluxes in riboflavin-producing Bacillus subtilis during growth on two-carbon substrate mixtures. Appl Environ Microbiol 2002; 68:1760–1771 [View Article] [PubMed]
    [Google Scholar]
  93. Hullin RP, Hassall H. The synthesis of cell constituents from butane-2,3-diol by Pseudomonas sp. Biochem J 1962; 83:298–303 [View Article] [PubMed]
    [Google Scholar]
  94. Bieri M. The environmental profile of metaldehyde. In BCPC Symposium Proceedings British Crop Protection Council; 2003 pp 255–262
    [Google Scholar]
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