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Microbiology of Reductive Dehalogenation: Something Old, Something New

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Microbiology of Reductive Dehalogenation: Something Old, Something New Microbiology of Reductive Dehalogenation: Something Old, Something New Steve Zinder MBL, June 19, 2013 Chlorinated organic compounds PCE TCE cis-DCE trans-DCE 1,1-DCE VC Aerobic Degradation of Chloroethenes H! H! mineralization! C!=!C! CO2! H! Cl! non specific! H! H! oxygenases! C!=!C! CO2, etc.! Cl! Cl! mineralization! (Strain JS666)! Cl! H! Cl! O! H! C!=!C! C!–C! ! Cl! Cl! Cl! Cl! Cl! Cl! toluene! C!=!C! ??! monooxygenase! Cl! Cl! Reductive dechlorination of PCE Cl Cl 2H HCl Cl H 2H HCl H H 2H HCl H H 2H HCl H H C C C C C C C C C C Cl Cl Cl Cl Cl Cl H Cl H H PCE TCE DCEs VC ETH James Gossett Known human carcinogen PCE conversion to ETH by a MeOH/PCE enrichment from the Ithaca Sewage Plant Hours Envir Sci Technol 28:973, 1994 H+/H 2 -0.4 - -0.3 Organochloride CO2/Acetate CO2/CH4 2- -0.2 respiration SO4 /H2S (halorespiration -0.1 dehalorespiration, 0.0 respiratory reductive +0.1 Fe(OH) /Fe(CO ) 3 3 +0.2 dechlorination) +0.3 cDCE/VC - - +0.4 NO3 /NO2 VC/ETH +0.5 TCE/cDCE PCE/TCE +0.6 - +0.7 NO3 /N2 +0.8 O2/H2O +0.9 3-Chlorobenzoate dehalogenating community Desulfomonile tiedjei Syntrophus Methanospirillum Methanosaeta Organisms reducing PCE and TCE to cDCE MeOH/PCE-dechlorinating culture Phase contrast Fluorescence, Xavier Maymó-Gatell “Dehalococcoides ethenogenes” strain 195 (Science, 276:1568, 1997) EM of Dhc strain 195 S-layer cell wall No peptido- glycan Methanosarcina! Sulfolobus! Planctomyces! Gloeobacter! Nostoc! Cyanobacteria! Mycoplasma! Clostridium! Dehalobacter restrictus! Desulfitobacterium.dehalogens! Desulfitobacterium.chlororespirans! Firmicutes ! Desulfitobacterium.frappieri ! Desulfitobacterium.hafniens! Desulfitobacterium StrainDCE! ! Actinomyces! Streptomyces! Actinobacteria! Desulfovibrio! Dehalospirillum multivorans! Desulfuromonas chloroethenica! Proteobacteria! Agrobacterium! Enterobacter MS1! ! Escherichia coli! Chloroflexus! Sphaerobacter! SJA15! TCB consortium! OPB12! Hot Spring! WCHB1.50!Chl. solvent aquifer! GCA112! WCHA1.69! Chl. solvent aquifer! OPB9! Hot spring! SJA170! TCB consortium! Chloroflexi! MUG9! Anaerobic bioreactors TUG8! ! H12f! Hanford, WA reactor! “GNS Bacteria”! SAR202! Sargasso sea! RFLP17! PCB consortium! Dehalococcoides ethenogenes! 16S rRNA gene vadinBA26! Wine waste reactor! ACE22! Antarctic lake! H3.93! t0.8.f! Hanford, WA aquifer! Phylogeny-2000 H1.4.f! MT61! 0.1! Dehalococcoides and relatives Dhc FL2, AF357918 Dhc GT, AY914178 Dhc CBDB1, AJ965256 Strain KB1-VC, AY146779 Pinellas Clone JN18_V35_B, EF059529 Dhc BAV1, AY165308 Dehalogenating Strain KB1-PCE, AY146780 All > 97% 16S ID Chloroflexi Dhc VS, AY323233 Victoria Dhc 195, AF004928 Strain TM-EtOH, AY882433 Cornell Dehalogenimonas lykanthroporepellens EU679418 Clone LaC15H20, EF667695 Dehalobium chlorocoercia Strain DF-1, AF393781 Clone SAR202, U20797 Clone H1.2.f,, AF005747 Marine Chloroflexi Clone FTL276, AF529110 Anaerolinea thermophila UNI-1, AB046413 Anaerolinea Caldilinea aerolinea, AB067647 Chloroflexus aurantiacus, M34116 “Classical” Chloroflexi Dehalococcoides mccartyi Perry McCarty with Tyler Prize for Environmental Achievement The real world: Site 1381 Cape Canaveral Air Station (CCAS) Amy Carroll detected Dhc with PCR Pump lactate as electron donor H2 Biostimulaton With Electron Donors Butyrate, Ethanol, Benzoate, Lactate, or Vegetable Oil PCE ETH H2 4 HCl Dechlorinators CO2 Methanogens Methane Acetate CO2 Bioremediation at Site 1381: fate of chloroethenes in a central well after adding lactate M ic h ig a n R iv e rs Red Cedar River Ki t c h n e r Père Marquertte River It h a c a Ke n t New a r k Au Sable River Niagara Falls Ft. Lewis Neeco Park (Niagara Falls) Textron (Niagara Falls) Alameda NAS P om p to n La k e s Oa k l e y Dover AFB LF 13 Lo r e n z Dover AFB Pilot S ac ra m en to Ja c k s o n v i l l e Wi n f i e l d Cape D o rd re c h t Kelly AFB LF Canaveral Am s te rd a m Kelly AFB Pilot Vi c t o r i a De Lisle C ent ra l Holland Berlin, GR Be a u m o n t Pi n e l l a s C he s h ir e , Cornell Labs Tiedje’s Lab N. England RTDFR Sites* Geosyntec* Stuttgart, GR Du Pont’s Sites* German Labs Compiled by Edwin R. Hendrickson, DuPont Company,CRD/CCER & CRG * Data Contributed by Edwin R. Hendrickson, DuPont Co. Commercial Dehalococcoides cultures for bioaugmentation Shaw Group SDC-9 + Bioremediation Consulting International (BCI) Labs, and Bioaug LLC + Zinder Lab, Summer 2001 Ivonne ! Nijenhuis! Amy! Carroll! Tim Anguish! Dehalococcoides ethenogenes genome •" Sequenced by the Institute for Genomic Research (JCVI) (funded by DOE)- •" John Heidelberg, Rekha Seshadri, and Derrick Fouts main collaborators 1 •" Size: 1,470,272 bp ≤ /3 that of E. coli •" %G+C = 48.9 •" Predicted protein-encoding ORFs: 1592 •" Similar to known function: 904 (56.7%) •" Similar to unknown function: 386 (24.3%) •" No match: 302 (19%) •" Seshadri et al. Science 307:105, 2005 TCE reductive dehalogenase (RD) A Corrinoid “Periplasm” 3-4Fe4S 4Fe4S Membrane TAT B RR PC C Twin arginine export signal Three FeS proline motif centers PCE RDH: PCE + 2H TCE + HCl TCE RDH: TCE + 4H VC + 2HCl ( ETH) Magnuson et al. AEM 66: 5141 (2000) Dehalococcoides! ethenogenes ! genome map-! RDs! DET0318! pceA 2C! Regs! %GC! Trinucs! GC! MarR! skew! = Mobile genetic elements ≈ 13.6% of genome Phage? 17 complete + 2 defective RDHs Most have adjacent two-component or MarR transcriptional regulators RDH homologues detected in PceA Dehalococcoides Chloro- A large (96) and phenols phylogenetically diverse family Only know functions for 5 TceA homologous groups BvcA-VC VcrA-VC CbrA - Chlorobenzenes RDHs from Firmicutes ACT comparison of genomes 17 RDHs 36 RDHs 32 RDHs HPR = high plasticity regions RDH genes in black RDH homologues in yellow Homologues transcribed in same direction in red, opposite direction in blue D. ethenogenes temperate phage •" Heather Fullerton has succeeded in growing Det in defined medium •" Genes (DET 1067-1104 encoding an ostensibly complete phage are found in the DET genome – related to G+ phages – no att site •" Phage particles can be detected by fluorescence and electron microscopy and appear to be 10-fold induced by mitomycin C Dehalococcoides: lessons learned •" Dehalococcoides “Born to dechlorinate” •" RDHs are a large phylogenetically deep gene family •" RDH genes usually found in “islands” of high genetic plasticity –"Housekeeping genes are syntenic and highly conserved between strains –"Fits core genome/pan genome model for species •" Reductive dehalogenation past DCE at a contaminated sites apparently requires the presence Dehalococcoides •" RDHs are better biomarkers for dehalogenation than 16S rRNA Chlorobenzenes •" Chlorobenzenes (CBs) used as chemical precursors, solvents, and pesticides •" Tons of monochlorobenzene (MCB) in groundwater at Montrose Chemical Plant in Fullerton CA – made DDT •" Diverse aerobes like Pseudomonas and Burkholderia can degrade DCBs and MCB –" Use well known oxygenase based aromatic degradation pathways 1,4-DCB in moth balls and CBs in car wax MCB used to Chlorobenzenes: anaerobic degradation •" CBs can form dense nonaqueous phase liquids (DNAPLs) that migrate to anaerobic zones •" Dehalococcoides CBDB1 and 195 reductively dehalogenate CBs with ≥3 Cl •" Dhc stop at TCBs and DCBs •" In ~2005 DuPont asked our lab to investigate reductive dehalogenation of DCBs and MCB •" Much less was known about anaerobic degradation of DCBs and MCB Model for anaerobic DCB dechlorination - 2005 CH4 , CO Trace amounts 2H HCl during DCB to MCB Methanogenic conditions Cl 2H HCl ortho)-dichlorobenzene 2- 3+ SO4 , Fe or - benzene NO3 -reducing conditions Cl Cl CO meta)-dichlorobenzene 2 monochlorobenzene 2- 3+ Cl SO4 , Fe or - NO3 -reducing CO2 Microcosms conditions slow rates Cl Solid arrows = known reactions Two early eras: Brian Weisenstein Jennifer Fung DuPont Chambers Works •" On Delaware River next to Memorial Bridge •" Dye factory in early 1900s - chloroanilines and CBs •" Samples came from a drainage ditch (DD) at the site •" Received on Dec 5, 2005 •" Brown mud with no detectable organic pollutants •" Dec 15- preliminary microcosm experiment – •" 20 g mud, •" 50 ml anoxic water, •" 3 DCB isomers DD •" yeast extract as electron donor •" GC readings at 1 day and at 20 days (after break) The Xmas miracle 100 90 80 70 12DCB 60 13DCB 14DCB 50 MCB umoles 40 Tol 30 Benz 20 10 0 0 10 20 30 40 50 60 Days CW microcosms: all three DCB isomers Fung et al. ES&T 43:2302 (2009) CW microcosms: individual CBs 1,2-DCB 1,3-DCB 1,4-DCB MCB DCBs: Culture experiments •" Jen Fung developed three enrichment cultures, one for each DCB isomer •" The 1,2-DCB culture was the fastest, so we studied it •" We expected Dehalococcoides to be the dehalogenator •" However, vancomycin inhibited 1,2-DCB dehalogenation– Dhc is resistant •" We couldn’t detect Dhc with specific 16S primers •" Made a 16S rRNA gene clone library with universal bacterial primers (Hinsby Cadillo-Quiroz) •" No Dhc, but > 25% of clones Dehalobacter Dehalobacter Firmicutes (Gram +) •" Dehalobacter restrictus PER-K23 PCE/ TCE to cis-DCE –" Requires B Vitamins, Arg, His, Thr for growth •" Dehalobacter strain TCA1 1,1,1-TriChloroethAne/1,1-DCA to CA •" Dehalobacter-containing mixed cultures –" 1,2-DCA to ethene –" Tetrachlorophthalide –" Hexachlorocyclohexane (Lindane) •" Specialists –" Only H2 or sometimes formate as electron donor –" Only chlorinated electron acceptors Optimizing the 1,2-DCB Enrichment •" Project was taken over by Jenny Nelson •" Goal is to make Dhb most numerous organism in culture •" Organic nutrients cut down to 2 mM acetate (C source), vitamins, and 20 mg/L
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