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Widespread Distribution of Dehalococcoides mccartyi in the Houston Ship Channel and Galveston Bay, Texas, Sediments and the Potential for Reductive Dechlorination of PCDD/F in an Estuarine Environment

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Abstract

Sediments in the Houston Ship Channel and upper Galveston Bay, Texas, USA, are polluted with polychlorinated dibenzo-p-dioxins/furans (PCDD/F; ≤46,000 ng/kg dry weight (wt.)) with 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), the most toxic congener, contributing >50 % of the total toxic equivalents (TEQ) at most locations. We measured PCDD/F concentrations in sediments and evaluated the potential for enhanced in situ biodegradation by surveying for Dehalococcoides mccartyi, an obligate organohalide respiring bacterium. Dehalococcoides spp. (98 % similar to D. mccartyi) and 22 other members of the class Dehalococcoidia were predominant 16S ribosomal RNA (rRNA) phylotypes. Dehalococcoides spp. were also present in the active fraction of the bacterial community. Presence/absence PCR screening detected D. mccartyi in sediment cores and sediment grab samples having at least 1 ng/kg dry wt. TEQ at salinities ranging from 0.6 to 19.5 PSU, indicating that they are widespread in the estuarine environment. Organic carbon-only and organic carbon + sulfate-amended sediment microcosm experiments resulted in ∼60 % reduction of ambient 2,3,7,8-TCDD in just 24 months leading to reductions in total TEQs by 38.4 and 45.0 %, respectively, indicating that 2,3,7,8-TCDD degradation is occurring at appreciable rates.

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References

  • Acinas SG, Sarma-Rupavtarm R, Klepac-Ceraj V, Polz MF (2005) PCR-induced sequence artifacts and bias: insights from comparison of two 16S rRNA clone libraries constructed from the same sample. Appl Environ Microbiol 71:8966–8969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adriaens P, Grbić-Galić D (1994) Reductive dechlorination of PCDD/F by anaerobic cultures and sediments. Chemosphere 29:2253–2259

    Article  CAS  Google Scholar 

  • Adrian L (2009) ERC-group microflex: microbiology of Dehalococcoides-like Chloroflexi. Rev Environ Sci Biotechnol. doi:10.1007/s11157-009-9166-y

    Google Scholar 

  • Adrian L, Dukova V, Demnerova K, Bedard DL (2009) Dehalococcoides strain CBDB1 extensively dechlorinates the commercial polychlorinated biphenyl (PCB) mixture Arochlor 1260. Appl Environ Microbiol 75:4516–4524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adrian L, Hansen SK, Fung JM, Goerisch H, Zinder SH (2007) Growth of Dehalococcoides strains with chlorophenols as electron acceptors. Environ Sci Technol 41:2318–2323

    Article  CAS  PubMed  Google Scholar 

  • Adrian L, Szewzyk U, Wecke J, Gorisch H (2000) Bacterial dehalorespiration with chlorinated benzenes. Nature 408:580–583

    Article  CAS  PubMed  Google Scholar 

  • Ahn Y-B, Häggblom MM, Fennell DE (2005) Co-amendment with halogenated compounds enhances anaerobic microbial dechlorination of 1,2,3,4-tetrachlorodibeno-p-dioxin and 1,2,3,4-tetrachlorodibenzofuran in estuarine sediments. Environ Tox Chem 24:2775–2784

    Article  CAS  Google Scholar 

  • Ahn Y-B, Häggblom MM, Kerkhof LJ (2007) Comparison of anaerobic microbial communities from estuarine sediments amended with halogenated compounds to enhance dechlorination of 1,2,3,4-tetrachlorodibenzo-p-dioxin. FEMS Microbiol Ecol 61:362–371

    Article  CAS  PubMed  Google Scholar 

  • Ahn Y-B, Liu F, Fennell DE, Häggblom MM (2008) Biostimulation and bioaugmentation to enhance dechlorination of polychlorinated dibenzo-p-dioxins in contaminated sediments. FEMS Microbiol Ecol 66:271–281

    Article  CAS  PubMed  Google Scholar 

  • Ballerstedt H, Hantke, J, Bunge M, Werner B, Gerritse J, Andreesen JR, Lechner (2004) Properties of trichlorodibenzo-p-dioxin-dechlorinating mixed culture with a Dehalococcoides as putative dechlorinating species. FEMS Microbiol Ecol 47:223–234

  • Bedard DL (2008) A case study for microbial biodegradation: anaerobic bacterial reductive dechlorination of polychlorinated biphenyls from sediment to defined medium. Annu Rev Microbiol 62:253–270

    Article  CAS  PubMed  Google Scholar 

  • Bedard DL, Ritalahti KM, Loeffler FE (2007) The Dehalococcoides population in sediment-free mixed cultures metabolically dechlorinates the commercial polychlorinated biphenyl mixture Aroclor 1260. Appl Environ Microbiol 73:2513–2521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berggren DRV, Marshall IPG, Azizian MF, Spormann AM, Semprini L (2013) Effects of sulfate reduction on the bacterial community and kinetic parameters of a dechlorinating culture under chemostat growth conditions. Environ Sci Technol 47:1879–1886

    Article  CAS  PubMed  Google Scholar 

  • Brinkmeyer R, Knittel K, Juergens J, Weyland H, Amann R, Helmke E (2003) Diveristy and structure of bacterial communities in Arctic versus Antarctic pack ice. Appl Environ Microbiol 69:6610–6619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bunge M, Adrian L, Kraus A, Opel M, Lorenz WG, Andreesen JR, Gorisch H, Lechner U (2003) Reductive dehalogenation of chlorinated dioxins by an anaerobic bacterium. Nature 421:357–360

    Article  CAS  PubMed  Google Scholar 

  • Bunge M, Wagner A, Fischer M, Andeesen JR, Lechner U (2008) Enrichment of a dioxin-dehalogenating Dehalococcoides species in two-liquid phase cultures. Environ Microbiol 10:2670–2683

    Article  CAS  PubMed  Google Scholar 

  • Burdige DJ (2006) Geochemistry of marine sediments. Princeton University Press, Princeton

    Google Scholar 

  • Coenye T, Vandamme P (2003) Intragenomic heterogeneity between multiple 16S ribosomal RNA operons in sequenced bacterial genomes. FEMS Microbiol Lett 228:45–49

    Article  CAS  PubMed  Google Scholar 

  • Cooper M, Wagner A, Wondrousch D, Sonntag F, Sonnabend A, Brehm M, Schüürmann G, Adrian L (2015) Anaerobic microbial transformation of halogenated aromatics and fate prediction using electron density modeling. Environ Sci Technol 49:6018–6028

    Article  CAS  PubMed  Google Scholar 

  • Duhamel M, Mo K, Edwards EA (2004) Characterization of a highly enriched Dehalococcoides-containing culture that grows on vinyl chloride and trichloroethene. Appl Environ Microbiol 70:5538–5545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fennell DE, Nijenhuis I, Wilson SF, Zinder SH, Haeggblom M (2004) Dehalococcoides ethenogenes strain 195 reductively dechlorinates diverse chlorinated aromatic pollutants. Environ Sci Technol 38:2075–2081

    Article  CAS  PubMed  Google Scholar 

  • Ferguson JF, Pietari JMH (2000) Anaerobic transformations and bioremediation of chlorinated solvents. Environ Pollut 107:209–215

    Article  CAS  PubMed  Google Scholar 

  • Field JA, Sierra-Alvarez R (2008) Microbial degradation of chlorinated dioxins. Chemosphere 71:1005–1018

    Article  CAS  PubMed  Google Scholar 

  • Grostern A, Edwards EA (2006) Growth of Dehalobacter and Dehalococcoides spp. during degradation of chlorinated ethanes. Appl Environ Microbiol 72:428–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo L, Santschi PH (1997) Measurements of dissolved organic carbon (DOC) in seawater by the high temperature combustion method. Acta Oceanol Sin 16:59–73

    Google Scholar 

  • Guo L, Coleman CH, Santschi PH (1994) The distribution of colloidal and dissolved organic carbon in the Gulf of Mexico. Mar Chem 45:105–119

    Article  CAS  Google Scholar 

  • Guo L, Santschi PH, Warnken KW (1995) Dynamics of dissolved organic carbon (DOC) in oceanic environments. Limnol Oceanogr 40:1392–1403

    Article  CAS  Google Scholar 

  • Harkness MR, Bracco AA, Brennan MJ, Deweerd KA, Spivack JL (1999) Use of bioaugmentation to stimulate complete reductive dechlorination of trichloroethene in dover soil columns. Environ Sci Technol 33:1100–1109

    Article  CAS  Google Scholar 

  • Hiraishi A (2003) Biodiversity of dioxin-degrading microorganisms and potential utilization in bioremediation. Microbes Environ 18:105–125

    Article  Google Scholar 

  • Hiraishi A (2008) Biodiversity of dehalorespiring bacteria with special emphasis on polychlorinated biphenyl/dioxin dechlorinators. Microbes Environ 23:1–12

    Article  PubMed  Google Scholar 

  • Hiraishi A, Kaiya S, Miyakoda H, Futamata H (2005a) Biotransformation of polychlorinated dioxins and microbial community dynamics in sediment microcosms at different contamination levels. Microbes Environ 20:227–242

    Article  Google Scholar 

  • Hiraishi A, Sakamaki N, Miyakoda H, Maruyama T, Kato K, Futamata H (2005b) Estimation of "Dehalococcoides" populations in lake sediment contaminated with low levels of polychlorinated dioxins. Microbes Environ 20:216–226

    Article  Google Scholar 

  • Hoelscher T, Krajmalnik-Brown R, Ritalahti KM, Von Wintzingerode F, Goerisch H, Loeffler F, Adrian L (2004) Multiple nonidentical reductive-dehalogenase-homologous genes are common in Dehalococcoides. Appl Environ Microbiol 70:5290–5297

    Article  CAS  Google Scholar 

  • Holliger C, Wohlfarth G, Diekert G (1999) Reductive dechlorination in the energy metabolism of anaerobic bacteria. FEMS Microbiol Rev 22:383–398

    Article  Google Scholar 

  • Holmes VF, He J, Lee PKH, Alvarez-Cohen L (2006) Discrimination of multiple Dehalococcoides strains in a trichloroethene enrichment of quantification of their reductive dehalogenase genes. Appl Environ Microbiol 72:5877–5883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hug LA, Maphosa F, Leys D, Loffler FE, Smidt H, Edwards EA, Adrian L (2013) Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases. Philos Trans R Soc Lond Ser B Biol Sci 368:1–10

    Article  Google Scholar 

  • Kao CM, Chen SC, Liu JK, Wu MJ (2001) Evaluation of TCDD biodegradability under different redox conditions. Chemosphere 44:1447–1454

    Article  CAS  PubMed  Google Scholar 

  • Kjellerup BV, Paul P, Ghosh U, May HD, Sowers KR (2012) Spatial distribution of PCB dechlorinating bacteria and activities in contaminated soil. Appl Environ Soil Sci 2012:1–11

  • Krumins V, Park J-W, Son E-K, Rodenburg L, Kerkhof LJ, Haggblom MM, Fennell DE (2009) PCB dechlorination enhancement in Anacostia River sediment microcosms. Water Res 43:4549–4558

    Article  CAS  PubMed  Google Scholar 

  • Kube M, Beck A, Zinder SH, Kuhl H, Reinhardt R, Adrian L (2005) Genome sequence of the chlorinated compound-respiring bacterium Dehalococcoides species strain CBDB1. Nat Biotechnol 23:1269–1273

    Article  CAS  PubMed  Google Scholar 

  • Lakshmanan D, Howell NL, Rifai HS, Koenig L (2010) Spatial and temporal variation of polychlorinated biphenyls in the Houston Ship Channel. Chemosphere 80:100–112

    Article  CAS  PubMed  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nuclei acids techniques in bacaterial systematics. John Wiley and Sons, Chichester, p 115–147

    Google Scholar 

  • Major DW, Mcmaster ML, Cox EE, Edwards EA, Dworatzek SM, Hendrickson ER, Starr MG, Payne JA, Buonamici LW (2002) Field demonstration of successful bioaugmentation to achieve dechlorination of tetrachloroethene to ethene. Environ Sci Technol 36:5106–5116

    Article  CAS  PubMed  Google Scholar 

  • Mass̩ol-Deya AA, Odelson DA, Hickey RF, Tiedje JM (1999) Bacterial community fingerprinting of amplified 16S and 16–23S ribosomal DNA gene sequences and restriction endonuclease analysis (ARDRA). In: Akkermans ADL, van Elsas JD, De Bruijn FJ (eds) Molecular microbial ecology manual. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Maymo-Gatell X, Chien YT, Gossett JM, Zinder SH (1997) Isolation of a bacterium that reductively delchlorinates tetrachlorethene to ethene. Science 276:1568–1571

    Article  CAS  PubMed  Google Scholar 

  • Millero FJ (1996) Chemical oceanography. CRC Press, Boca Raton

    Google Scholar 

  • Mitchell KN (2009) Depth-utilization analysis for estimating economic activity supported by dredging. Terra et Aqua 116:22–30

    Google Scholar 

  • Moe WM, Yan J, Nobre MF, da Costa MS, Rainey FA (2009) Dehalogenimonas lykanthroporepellens gen. nov., sp. nov., a reductive dehalogenating bacterium isolated from chlorinated solvent contaminated groundwater. Int J Syst Evol Microbiol 59:2692–2697

  • Mullins TD, Britschgi TB, Krest RL, Giovannoni SJ (1995) Genetic comparisons reveal the same unknown bacterial lineages in Atlantic and Pacific bacterioplankton communities. Appl Environ Microbiol 40:148–158

    CAS  Google Scholar 

  • Narihiro T, Kaiya S, Futamata H, Hiraishi A (2010) Removal of polychlorinated dioxins by semi-aerobic fed-batch composting with biostimulation of “Dehalococcoides”. J Biosci Bioeng 109:249–256

    Article  CAS  PubMed  Google Scholar 

  • Nogales B, Moore ERB, Abraham W-R, Timmis KN (1999) Identification of the metabolically active members of a bacterial community in a polychlorinated biphenyl-polluted moorland soil. Environ Microbiol 1:199–212

    Article  CAS  PubMed  Google Scholar 

  • Payne RB, Fagervold SK, May HD, Sowers KR (2013) Remediation of polychlorinated biphenyl impacted sediment by concurrent bioaugmentation with anaerobic halorespiring and aerobic degrading bacteria. Environ Sci Technol 47:3807–3815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • POH (2014) Port of Houston Economic Impact. http://www.portofhouston.com/about-us/economic-impact/. Accessed 15 May 2014

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Gloeckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  CAS  PubMed  Google Scholar 

  • Quensen JF, Mueller SA, Jain MK, Tiedje JM (1998) Reductive dechlorination of DDE to DDMU in marine sediment microcosms. Science 280:722–724

    Article  CAS  PubMed  Google Scholar 

  • Quensen JF, Tiedje JM, Jain MK, Mueller SA (2001) Factors controlling the rate of DDE dechlorination to DDMU in Palos Verdes margin sediments under anaerobic conditions. Environ Sci Technol 35:286–291

    Article  CAS  PubMed  Google Scholar 

  • Ravinsan DA, Gupta RS (2014) Molecular signatures for members of the genus Dehalococcoides and the class Dehalococcoidia. Int J Syst Evol Microbiol 64:2176–2181

    Article  Google Scholar 

  • Richardson RE (2013) Genomic insights into organohalide respiration. Curr Opin Biotechnol 24:498–505

    Article  CAS  PubMed  Google Scholar 

  • Rifai H, Palachek R, Jensen P (2006) Total Maximum Daily Loads for Dioxins in the Houston Ship Channel. http://www.tceq.texas.gov/waterquality/tmdl/26-hscdioxin.html. Accessed 15 May 2014

  • Santschi PH, Yeager KM, Brinkmeyer R, Louchouarn P (2009) Factors regulating microbial degradation of dioxins in estuarine sediments: Houston Ship Channel and Galveston Bay, Texas. Final report to Texas Seagrant (http://texasseagrant.org/)

  • Sowers KR, May HD (2013) In situ treatment of PCBs by anaerobic microbial dechlorination in aquatic sediment: are we there yet? Curr Opin Biotechnol 24:482–488

    Article  CAS  PubMed  Google Scholar 

  • Stringer R, Johnston P (2001) Chlorine and the environment: an overview of the chlorine industry. Kluwer Academic Publishers, Dordrecht

    Book  Google Scholar 

  • Suarez MP, Rifai H, Palachek R, Dean K, Koenig L (2006) Distribution of polychlorinated dibenzo-p-dioxins and dibenzofurans in suspended sediments, dissolved phase and bottom sediment in the Houston Ship Channel. Chemosphere 62:417–429

    Article  CAS  PubMed  Google Scholar 

  • Sung Y, Fletcher KE, Ritalahti KM, Apkarian RP, Ramos-Hernandez N, Sanford RA, Mesbah NM, Loeffler FE (2006) Geobacter lovleyi sp. nov. strain SZ, a novel metal-reducing and tetrachlorethene-dechlorinating bacterium. Appl Environ Microbiol 72:2775–2782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tas N, Eekert MHA, De Vos WM, Smidt H (2010) The little bacteria that can - diversity, genomics, and ecophysiology of ‘Dehalococcoides’ spp. in contaminated environments. Microb Biotechnol 3:389–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • USEPA (2000) Engineered approaches to in situ bioremediation of chlorinated solvents: fundamentals and field applications. U.S. Environmental Protection Agency, Washington, DC

    Google Scholar 

  • USEPA (2014) San Jacinto River Waste Pits. http://www.epa.gov/region6/6sf/texas/san_jacinto/. Accessed 15 May 2014

  • Warnken KW, Gill GA, Santschi PH, Griffin LL (2000) Benthic exchange of nutrients in Galveston Bay, Texas. Estuaries 23:647–661

    Article  CAS  Google Scholar 

  • Weber R, Gaus C, Tysklind M, Johnston P, Forter M, Hollert H, Heinisch E, Holoubek I, Lloyd-Smith M, Masunaga S, Moccarell P, Santillo D, Selke N, Symons R, Torres JPM, Verta M, Varbelow G, Vijgen J, Watson A, Costner P, Woelz J, Wyclsk P, Zennegg M (2008) Dioxin- and POP-contaminated sites-contemporary and future relevance and challenges. Environ Sci Pollut Res 15:363–393

    Article  CAS  Google Scholar 

  • Wright ES, Yilmaz LS, Noguera DR (2012) DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl Environ Microbiol 78:717–725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan T, Lapara TM, Novak PJ (2006) The reductive dechlorination of 2,3,4,5-tetrachlorobiphenyl in three different sediment cultures: evidence for the involvement of phylogenetically similar Dehalococcoides-like bacteria populations. FEMS Microbiol Ecol 55:248–261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeager KM, Santschi PH (2003) Invariance of isotope ratios of lithogenic radionuclides: more evidence for their use as sediment source tracers. J Environ Radioact 69(3):159–176

  • Yeager KM, Santschi PH, Rifai H, Suarez MP, Brinkmeyer R, Hung CC, Schindler KJ, Andres MJ, Weaver E (2007) Dioxin chronology and fluxes in sediments of the Houston Ship Channel, Texas: influences of non-steady-state sediment transport and total organic carbon. Environ Sci Technol 41:5291–5298

    Article  CAS  PubMed  Google Scholar 

  • Yoshida N, Takahashi N, Hiraishi A (2005) Phylogenetic characterization of a polychlorinated-dioxin-dechlorinating microbial community by use of microcosm studies. Appl Environ Microbiol 71:4325–4334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zar J (1984) Biostatistical analysis. Prentice-Hall, Englewood Cliffs

  • Zhou JZ, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–332

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study was funded by a Texas Seagrant Program award to PHS, RB, and KMY and a Texas Commission on Environmental Quality award to RB. A special thank you to Erik Wright for assistance with DECIPHER. We also thank Dr. Lorenz Adrian for D. mccartyi strain CBDB1 DNA.

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Correspondence to Anne-Sophie Charlotte Hieke.

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Electronic Supplementary Material

Table S1

PCDD/F concentrations (ng/kg dry wt.) in sediment cores with D. mccartyi presence (+)/absence (−) data. PCR inhibition is designated with an “i.” (DOCX 98 kb)

Table S2

H2S (μmol l−1) in SG sediment core pore water (Santschi et al. 2009). (DOCX 99 kb)

Table S3

Salinity (PSU) in SG sediment core pore water. (DOCX 77 kb)

Table S4

Total organic carbon (TOC), dissolved organic carbon (DOC), and inorganic carbon (IC) in pore water for sediment cores SG1, SG3, and SG4. (DOCX 61 kb)

Table S5

Total organic carbon (TOC), dissolved organic carbon (DOC), and inorganic carbon (IC) in pore water for sediment cores SG6, SG7, and SG8. (DOCX 57 kb)

Table S6

POC (mg g−1) in SG sediment cores. (DOCX 69 kb)

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Hieke, AS.C., Brinkmeyer, R., Yeager, K.M. et al. Widespread Distribution of Dehalococcoides mccartyi in the Houston Ship Channel and Galveston Bay, Texas, Sediments and the Potential for Reductive Dechlorination of PCDD/F in an Estuarine Environment. Mar Biotechnol 18, 630–644 (2016). https://doi.org/10.1007/s10126-016-9723-7

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