Identification of Two Organohalide-respiring Dehalococcoidia Associated to Different Dechlorination Activities in PCB-impacted Marine Sediments

Overview

Journal Microb Cell Fact

Publisher Biomed Central

Specialties Biotechnology
Microbiology

Date 2017 Jul 26

PMID 28738864

Citations 4

Authors

Andrea Nuzzo

Andrea Negroni

Giulio Zanaroli

Fabio Fava

Affiliations

Soon will be listed here.

Abstract

Background: Microbial reductive dechlorination of polychlorinated biphenyls (PCBs) plays a major role in detoxifying anoxic contaminated freshwater and marine sediments from PCBs. Known members of the phylum Chloroflexi are typically responsible for this activity in freshwater sediments, whereas less is known about the microorganisms responsible for this activity in marine sediments. PCB-respiring activities were detected in PCB-impacted marine sediments of the Venice Lagoon. The aim of this work was to identify the indigenous organohalide-respiring microorganisms in such environments and assess their dechlorination specificity against spiked Aroclor™ 1254 PCBs under laboratory conditions resembling the in situ biogeochemistry.

Results: High PCB dechlorination activities (from 150 ± 7 to 380 ± 44 μmol of chlorine removed kg week) were detected in three out of six sediments sampled from different locations of the lagoon. An uncultured non-Dehalococcoides phylotype of the class Dehalococcoidia closely related to Dehalobium chlorocoercia DF-1, namely phylotype VLD-1, was detected and enriched up to 10 16S rRNA gene copies per gram of sediment where dechlorination activities were higher and 25-4/24-4 and 25-2/24-2/4-4 chlorobiphenyls (CB) accumulated as the main tri-/dichlorinated products. Conversely, a different phylotype closely related to the SF1/m-1 clade, namely VLD-2, also enriched highly where lower dechlorination activity and the accumulation of 25-3 CB as main tri-chlorinated product occurred, albeit in the simultaneous presence of VLD-1. Both phylotypes showed growth yields higher or comparable to known organohalide respirers and neither phylotypes enriched in sediment cultures not exhibiting dechlorination.

Conclusions: These findings confirm the presence of different PCB-respiring microorganisms in the indigenous microbial communities of Venice Lagoon sediments and relate two non-Dehalococcoides phylotypes of the class Dehalococcoidia to different PCB dechlorination rates and specificities.

Citing Articles

Chemical and microbiological insights into two littoral Antarctic demosponge species: () (Topsent 1901) and () (Kirkpatrick 1907).

Papale M, Giannarelli S, Azzaro di Rosamarina M, Ghezzi L, Lo Giudice A, Rizzo C Front Microbiol. 2024; 15:1341641.

PMID: 38404594 PMC: 10884823. DOI: 10.3389/fmicb.2024.1341641.

Salinity determines performance, functional populations, and microbial ecology in consortia attenuating organohalide pollutants.

Xu G, Zhao X, Zhao S, Rogers M, He J ISME J. 2023; 17(5):660-670.

PMID: 36765150 PMC: 10119321. DOI: 10.1038/s41396-023-01377-1.

Structure and diversity of native bacterial communities in soils contaminated with polychlorinated biphenyls.

Zenteno-Rojas A, Martinez-Romero E, Castaneda-Valbuena D, Rincon-Molina C, Ruiz-Valdiviezo V, Meza-Gordillo R AMB Express. 2020; 10(1):124.

PMID: 32651884 PMC: 7351888. DOI: 10.1186/s13568-020-01058-8.

Bacterial Diversity and the Geochemical Landscape in the Southwestern Gulf of Mexico.

Godoy-Lozano E, Escobar-Zepeda A, Raggi L, Merino E, Gutierrez-Rios R, Juarez K Front Microbiol. 2018; 9:2528.

PMID: 30405581 PMC: 6200919. DOI: 10.3389/fmicb.2018.02528.

References

Read S, Marzorati M, Guimaraes B, Boon N . Microbial Resource Management revisited: successful parameters and new concepts. Appl Microbiol Biotechnol. 2011; 90(3):861-71. DOI: 10.1007/s00253-011-3223-5. View

Wang S, Chng K, Wilm A, Zhao S, Yang K, Nagarajan N . Genomic characterization of three unique Dehalococcoides that respire on persistent polychlorinated biphenyls. Proc Natl Acad Sci U S A. 2014; 111(33):12103-8. PMC: 4142991. DOI: 10.1073/pnas.1404845111. View

Watts J, Fagervold S, May H, Sowers K . A PCR-based specific assay reveals a population of bacteria within the Chloroflexi associated with the reductive dehalogenation of polychlorinated biphenyls. Microbiology (Reading). 2005; 151(Pt 6):2039-2046. DOI: 10.1099/mic.0.27819-0. View

Zanaroli G, Balloi A, Negroni A, Borruso L, Daffonchio D, Fava F . A Chloroflexi bacterium dechlorinates polychlorinated biphenyls in marine sediments under in situ-like biogeochemical conditions. J Hazard Mater. 2012; 209-210:449-57. DOI: 10.1016/j.jhazmat.2012.01.042. View

Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden T . Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics. 2012; 13:134. PMC: 3412702. DOI: 10.1186/1471-2105-13-134. View

Zhen H, Du S, Rodenburg L, Mainelis G, Fennell D . Reductive dechlorination of 1,2,3,7,8-pentachlorodibenzo-p-dioxin and Aroclor 1260, 1254 and 1242 by a mixed culture containing Dehalococcoides mccartyi strain 195. Water Res. 2014; 52:51-62. DOI: 10.1016/j.watres.2013.12.038. View

Wiegel , Wu . Microbial reductive dehalogenation of polychlorinated biphenyls. FEMS Microbiol Ecol. 2000; 32(1):1-15. DOI: 10.1111/j.1574-6941.2000.tb00693.x. View

Bedard D, Ritalahti K, Loffler F . The Dehalococcoides population in sediment-free mixed cultures metabolically dechlorinates the commercial polychlorinated biphenyl mixture aroclor 1260. Appl Environ Microbiol. 2007; 73(8):2513-21. PMC: 1855590. DOI: 10.1128/AEM.02909-06. View

Kaya D, Imamoglu I, Dilek Sanin F, Payne R, Sowers K . Potential risk reduction of Aroclor 1254 by microbial dechlorination in anaerobic Grasse River sediment microcosms. J Hazard Mater. 2016; 321:879-887. DOI: 10.1016/j.jhazmat.2016.10.009. View

10.

May H, Miller G, Kjellerup B, Sowers K . Dehalorespiration with polychlorinated biphenyls by an anaerobic ultramicrobacterium. Appl Environ Microbiol. 2008; 74(7):2089-94. PMC: 2292607. DOI: 10.1128/AEM.01450-07. View

11.

Carpenter D . Polychlorinated biphenyls (PCBs): routes of exposure and effects on human health. Rev Environ Health. 2006; 21(1):1-23. DOI: 10.1515/reveh.2006.21.1.1. View

12.

Fava F, Zanaroli G, Young L . Microbial reductive dechlorination of pre-existing PCBs and spiked 2,3,4,5,6-pentachlorobiphenyl in anaerobic slurries of a contaminated sediment of Venice Lagoon (Italy). FEMS Microbiol Ecol. 2009; 44(3):309-18. DOI: 10.1016/S0168-6496(03)00069-2. View

13.

Ho C, Liu S . Effect of coplanar PCB concentration on dechlorinating microbial communities and dechlorination in estuarine sediments. Chemosphere. 2010; 82(1):48-55. DOI: 10.1016/j.chemosphere.2010.10.012. View

14.

Cutter L, Watts J, Sowers K, May H . Identification of a microorganism that links its growth to the reductive dechlorination of 2,3,5,6-chlorobiphenyl. Environ Microbiol. 2002; 3(11):699-709. DOI: 10.1046/j.1462-2920.2001.00246.x. View

15.

Marzorati M, Wittebolle L, Boon N, Daffonchio D, Verstraete W . How to get more out of molecular fingerprints: practical tools for microbial ecology. Environ Microbiol. 2008; 10(6):1571-81. DOI: 10.1111/j.1462-2920.2008.01572.x. View

16.

Wong C, Mabury S, Whittle D, Backus S, Teixeira C, DeVault D . Organochlorine compounds in Lake Superior: chiral polychlorinated biphenyls and biotransformation in the aquatic food web. Environ Sci Technol. 2004; 38(1):84-92. DOI: 10.1021/es0346983. View

17.

Zanaroli G, Balloi A, Negroni A, Daffonchio D, Young L, Fava F . Characterization of the microbial community from the marine sediment of the Venice lagoon capable of reductive dechlorination of coplanar polychlorinated biphenyls (PCBs). J Hazard Mater. 2010; 178(1-3):417-26. DOI: 10.1016/j.jhazmat.2010.01.097. View

18.

Kjellerup B, Sun X, Ghosh U, May H, Sowers K . Site-specific microbial communities in three PCB-impacted sediments are associated with different in situ dechlorinating activities. Environ Microbiol. 2008; 10(5):1296-309. DOI: 10.1111/j.1462-2920.2007.01543.x. View

19.

Fricker A, LaRoe S, Shea M, Bedard D . Dehalococcoides mccartyi strain JNA dechlorinates multiple chlorinated phenols including pentachlorophenol and harbors at least 19 reductive dehalogenase homologous genes. Environ Sci Technol. 2014; 48(24):14300-8. DOI: 10.1021/es503553f. View

20.

Fagervold S, May H, Sowers K . Microbial reductive dechlorination of aroclor 1260 in Baltimore harbor sediment microcosms is catalyzed by three phylotypes within the phylum Chloroflexi. Appl Environ Microbiol. 2007; 73(9):3009-18. PMC: 1892865. DOI: 10.1128/AEM.02958-06. View