Environmental compartments polluted with animal charcoal from the skin and hide cottage industries are rich in toxic heavy metals and diverse hydrocarbon classes, some of which are carcinogenic, mutagenic, and genotoxic, and thus require a bio-based eco-benign decommission strategies. A shotgun metagenomic approach was used to decipher the microbiome, hydrocarbon degradation genes, and heavy metal resistome of a microbial consortium (FN8) from an animal-charcoal polluted site enriched with fluorene. Structurally, the FN8 microbial consortium consists of 26 phyla, 53 classes, 119 orders, 245 families, 620 genera, and 1021 species. The dominant phylum, class, order, family, genus, and species in the consortium are Proteobacteria (51.37%), Gammaproteobacteria (39.01%), Bacillales (18.09%), Microbulbiferaceae (11.65%), Microbulbifer (12.21%), and Microbulbifer sp. A4B17 (19.65%), respectively. The microbial consortium degraded 57.56% (28.78 mg/L) and 87.14% (43.57 mg/L) of the initial fluorene concentration in 14 and 21 days. Functional annotation of the protein sequences (ORFs) of the FN8 metagenome using the KEGG GhostKOALA, KofamKOALA, NCBI's conserved domain database, and BacMet revealed the detection of hydrocarbon degradation genes for benzoate, aminobenzoate, polycyclic aromatic hydrocarbons (PAHs), chlorocyclohexane/chlorobenzene, chloroalkane/chloroalkene, toluene, xylene, styrene, naphthalene, nitrotoluene, and several others. The annotation also revealed putative genes for the transport, uptake, efflux, and regulation of heavy metals such as arsenic, cadmium, chromium, mercury, nickel, copper, zinc, and several others. Findings from this study have established that members of the FN8 consortium are well-adapted and imbued with requisite gene sets and could be a potential bioresource for on-site depuration of animal charcoal polluted sites.

Department of Biological Sciences Microbiology unit Elizade University Ilara Mokin Ondo State Nigeria

Zobrazit více v PubMed

Ahamed F, Hasibullah M, Ferdouse J, Anwar MN (2010) Microbial degradation of petroleum hydrocarbon. Bangladesh J Microbiol 27(1):10–13 DOI

Aislabie J, Deslippe JR (2013) Soil microbes and their contribution to soil services. In: Dymond JR (ed) Ecosystem services in New Zealand-conditions and trends. Manaaki Whenua Press, Lincoln, pp 143–161

Altenschmidt U, Fuchs G (1992) Novel aerobic 2-aminobenzoate metabolism. Purification and characterization of 2-aminobenzoate-CoA ligase, localization of the gene on a 8-kbp plasmid, and cloning and sequencing of the gene from a denitrifying Pseudomonas sp. Eur J Biochem 205:721–727 PubMed DOI

Anjem A, Imlay JA (2012) Mononuclear iron enzymes are primary targets of hydrogen peroxide stress. J Biol Chem 287(22411989):15544–15556 PubMed DOI PMC

Aramaki T, Blanc-Mathieu R, Endo H, Ohkubo K, Kanehisa M, Goto S, Ogata H (2020) KofamKOALA: KEGG ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics 36(7):2251–2252 PubMed DOI

Arnesano F, Banci L, Bertini I, Thompsett AR (2002) Solution structure of CopC: a cupredoxin-like protein involved in copper homeostasis. Structure 10:1337–1347 PubMed DOI

ATSDR (2005) Agency for Toxic Substances and Disease Registry, U.S. Department of Health, and Human Services. Toxicologic profile for alpha-, beta, gamma- and delta-hexachlorocyclohexane

Ausuri J, Vitale GA, Coppola D, Esposito FP, Buonocore C, de Pascale D (2021) Assessment of the degradation potential and genomic insights towards phenanthrene by Dietzia psychralcaliphila JI1D. Microorganisms 9(6):1327 PubMed DOI PMC

Belleret HR, Kane SR, Legler TC et al (2002) A real-time polymerase chain reaction method for monitoring anaerobic, hydrocarbon degrading bacteria based on a catabolic gene. Environ Sci Technol 36:3977–84 DOI

Ben Fekih I, Zhang C, Li YP, Zhao Y, Alwathnani HA, Saquib Q, Rensing C, Cervantes C (2018) Distribution of arsenic resistance genes in prokaryotes. Front Microbiol 9:2473 PubMed DOI PMC

Bihari Z, Szvetnik A, Szabó Z, Blastyák A, Zombori Z, Balázs M, Kiss I (2011) Functional analysis of long-chain n-alkane degradation by Dietzia spp. FEMS Microbiol Lett 316(2):100–107 PubMed DOI

Black CA (1965) Methods of Soil Analysis No. 9, Part 2. American Society of Agronomy, Madison, Wisconsin

Bødtker G, Hvidsten IV, Barth T, Torsvik T (2009) Hydrocarbon degradation by Dietzia sp. A14101 isolated from an oil reservoir model column. Antonie Van Leeuwenhoek 96(4):459–469

Boldrin B, Tiehm A, Fritzsche C (1993) Degradation of phenanthrene, fluorene, fluoranthene, and pyrene by a Mycobacterium sp. Appl Environ Microbiol 59:1927–1930 PubMed DOI PMC

Bondarczuk K, Piotrowska-Seget Z (2013) Molecular basis of active copper resistance mechanisms in Gram-negative bacteria. Cell Biol Toxicol 29(6):397–405 PubMed DOI PMC

Bray RH, Kurtz LT (1945) Determination of total organic and available forms of phosphorus in soils. Soil Sci. 59:39–45 DOI

Brito EMS, Guyoneaud R, Goñi-Urriza M, Ranchou-Peyruse A, Verbaere A, Crapez MA, Wasserman JC, Duran R (2006) Characterization of hydrocarbonoclastic bacterial communities from mangrove sediments in Guanabara Bay. Brazil. Res Microbiol 157(8):752–762 PubMed

Cai M, Xun L (2002) Organization and regulation of pentachlorophenol-degrading genes in Sphingobium chlorophenolicum ATCC 39723. J Bacteriol 184:4672–4680 PubMed DOI PMC

Cao B, Nagarajan K, Loh KC (2009) Biodegradation of aromatic compounds: current status and opportunities for biomolecular approaches. Appl Microbiol Biotechnol 85:207–28 PubMed DOI

Casellas M, Grifoll M, Bayona JM, Solanas AM (1997) New metabolites in the degradation of fluorene by Arthrobacter sp. strain F101. Appl Environ Microbiol 63:819–826 PubMed DOI PMC

Chen K, Zhu Q, Qian Y et al (2013) Microcalorimetric investigation of the effect of non-ionic surfactant on biodegradation of pyrene by PAH-degrading bacteria Burkholderia cepacia. Ecotoxicol Environ Saf 98:361–7 PubMed DOI

Chen L, Yang J (2008) Biochemical characterization of the tetrachlorobenzoquinone reductase involved in the biodegradation of pentachlorophenol. Int J Mol Sci 9:198–212 PubMed DOI PMC

Chopra SL, Kanwar JS (1998) Analytical Agricultural Chemistry. MacMillian Press, London

Dai X, Yan G, Guo S (2017) Characterization of Dietzia cercidiphylli C-1 isolated from extra-heavy oil contaminated soil. RSC adv 7:19486–19491 DOI

Elder DJE, Kelly DJ (1994) The bacterial degradation of benzoic acid and benzenoid compounds under anaerobic conditions: unifying trends and new perspectives. FEMS Microbiol Rev 13(4):441–468 PubMed DOI

Feknous N, Branes Z, Batisson I, Amblard C (2019) Growth of indigenous bacteria Vibrio alginolyticus and Dietzia sp. isolated from the East Coast of Algeria in the presence of monoaromatic hydrocarbons. Environ Protect Eng 45(3):127–137

Fox TC, Guerinot ML (1998) Molecular biology of cation transport in plants. Annu Rev Plant Physiol Plant Mol Biol 49:669–696 PubMed DOI

Franke S, Grass G, Rensing C, Nies DH (2003) Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J Bacteriol 185:3804–3812 PubMed DOI PMC

Ghosal D, Ghosh S, Dutta TK, Ahn Y (2016) Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): a review. Front Microbiol 7:1369 PubMed PMC

González JM, Mayer F, Moran MA, Hodson RE, Whitman WB (1997) Microbulbifer hydrolyticus Gen. Nov., Sp. Nov., and Marinobacterium georgiense Gen. Nov., Sp. Nov., two marine bacteria from a lignin-rich pulp mill-waste enrichment community. Int J Syst Bacteriol 47:369–376 PubMed DOI

González JM, Whitman WB (2006) Oceanospirillum and related genera. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (Eds), The Prokaryotes, A Handbook on the Biology of Bacteria. Third Edition, Vol. 6, Springer, 6:887–915

Graziano M, Rizzo C, Michaud L, Porporato EMD, De Domenico E, Spano N, Lo Giudice A (2016) Biosurfactant production by hydrocarbon-degrading Brevibacterium and Vibrio isolates from sea pen Pteroeides spinosum (Ellis, 1764). J Basic Microbiol 56(9):963–974 PubMed DOI

Grifoll M, Selifonov SA, Chapman PJ (1994) Evidence for a novel pathway in the degradation of fluorene by Pseudomonas sp. strain F274. Appl Environ Microbiol 60:2438–2449 PubMed DOI PMC

Grifoll M, Selifonov SA, Gatlin CV, Chapman PJ (1995) Actions of a versatile fluorene-degrading bacterial isolate on polycyclic aromatic hydrocarbons. Appl Environ Microbiol 61:3711–3723 PubMed DOI PMC

Gutierrez T (2017) Marine aerobic hydrocarbon-degrading Gammaproteobacteria: an overview. In: McGenity T (eds) Taxonomy, Genomics and Ecophysiology of Hydrocarbon-Degrading Aerobes. Handbook of Hydrocarbon and Lipid Microbiology. Springer, Cham. https://doi.org/10.1007/978-3-319-60053-6_22-1

Habe H, Ashikawa Y, Saiki Y, Yoshida T, Nojiri H, Omori T (2002) Sphingomonas sp. strain KA1, carrying a carbazole dioxygenase gene homologue, degrades chlorinated dibenzo-p-dioxins in soil. FEMS Microbiol Lett 211:43–49 PubMed DOI

Habe H, Chung JS, Kato H et al (2004) Characterization of the upper pathway genes for fluorene metabolism in Terrabacter sp. strain DBF63. J Bacteriol 186:5938–5944 PubMed DOI PMC

He P, Li L, Liu J, Bai Y, Fang X (2016) Diversity and distribution of catechol 2,3-dioxygenase genes in surface sediments of the Bohai Sea. FEMS Microbiol Lett 363(10):fnw086

Hedlund BP, Staley JT (2001) Vibrio cyclotrophicus sp. nov., a polycyclic aromatic hydrocarbon (PAH)-degrading marine bacterium. Int J Syst Evol Microbiol 51(Pt 1):61-66

Hobman JL, Brown NL (1996) Overexpression of MerT, the mercuric ion transport protein of transposon Tn501, and genetic selection of mercury hypersensitivity mutations. Mol Gen Genet 250:129–134 PubMed

Hobman JL, Crossman LC (2014) Bacterial antimicrobial metal ion resistance. J Med Microbiol 64:471–497 PubMed DOI

Imron MF, Titah HS (2018) Optimization of diesel biodegradation by Vibrio alginolyticus using Box-Behnken design. Environ Eng Res 23(4):374–382 DOI

Junca H, Pieper DH (2003) Amplified functional DNA restriction analysis to determine catechol 2,3- dioxygenase gene diversity in soil bacteria. J Microbiol Methods 55:697–708 PubMed DOI

Kamimura N, Takahashi K, Mori K et al (2017) Bacterial catabolism of lignin-derived aromatics: new findings in a recent decade: update on bacterial lignin catabolism. Environ Microbiol Rep 9(6):679–705 PubMed DOI

Kanaly RA, Harayama S (2010) Advances in the field of high molecular-weight polycyclic aromatic hydrocarbon biodegradation by bacteria. Microbiol Biotechnol 3(2):132–164 DOI

Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and Ghost-KOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428(4):726–731 PubMed DOI

Kasuga I, Nakajima F, Furumai H (2007) Diversity of catechol 2,3-dioxygenase genes of bacteria responding to dissolved organic matter derived from different sources in a eutrophic lake. FEMS Microbiol Ecol 61:449–58 PubMed DOI

Kieth LH, Teillard WA (1979) Priority pollutants: a perspective view. Environ Sci Technol 13:416–423 DOI

Kim D, Song L, Breitwieser FP, Salzberg SL (2016) Centrifuge: rapid and sensitive classification of metagenomic sequences. Genome Res 26:1721–1729 PubMed DOI PMC

Kim D, Yoo M, Kim E, Hong SG (2015) Anthranilate degradation by a cold-adapted Pseudomonas sp. J Basic Microbiol 55:354–362 PubMed DOI

Kiyono M, Sone Y, Nakamura R, Pan-Hou H, Sakabe K (2009) The MerE protein encoded by transposon Tn21 is a broad mercury transporter in Escherichia coli. FEBS Lett 583:1127–1131 PubMed DOI

Kumar S, Upadhayay SK, Kumari B, Tiwari S, Singh SN, Singh PK (2011) In vitro degradation of fluoranthene by bacteria isolated from petroleum sludge. Bioresour Technol 102:3709–3715 PubMed DOI

Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie-2. Nat Methods 9:357–359 PubMed DOI PMC

Larkin MJ, Kulakov LA, Allen CC (2005) Biodegradation and Rhodococcus- masters of catabolic versatility. Curr Opin Biotechnol 16:282–290 PubMed DOI

Lillis L, Clipson N, Doyle E (2010) Quantification of catechol dioxygenase gene expression in soil during degradation of 2,4-dichlorophenol. FEMS Microbiol Ecol 73:363–9 PubMed

Lisher JP, Giedroc DP (2013) Manganese acquisition and homeostasis at the host-pathogen interface. Front Cell Infect Microbiol 3(24367765):91 PubMed PMC

Lo C-C, Chain PSG (2014) Rapid evaluation and quality control of next generation sequencing data with FaQCs. BMC Bioinform 15:366 DOI

Lund PA, Brown NL (1987) Role of the merT and merP gene products of transposon Tn501 in the induction and expression of resistance to mercuric ions. Gene 52:207–214 PubMed DOI

Marchler-Bauer A, Derbyshire MK, Gonzales NR et al (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43(D):222–226

Martin JE, Giedroc DP (2016) Functional determinants of metal ion transport and selectivity in paralogous cation diffusion facilitator transporters CzcD and MntE in Streptococcus pneumoniae. J Bacteriol 198(26787764):1066–1076 PubMed DOI PMC

Medlar AJ, Törönen P, Holm L (2018) AAI-profiler: fast proteome-wide exploratory analysis reveals taxonomic identity, misclassification, and contamination. Nucleic Acids Res 46(W1):W479–W485 PubMed DOI PMC

Moghadam MS, Ebrahimipour G, Abtahi B, Ghassempour A, Hashtroudi MS (2014) Biodegradation of polycyclic aromatic hydrocarbons by a bacterial consortium enriched from mangrove sediments. J Environ Health Sci Eng 12:114 DOI

Monna L, Omori T, Kodama T (1993) Microbial degradation of dibenzofuran, fluorene, and dibenzo-p-dioxin by Staphylococcus auriculans DBF63. Appl Environ Microbiol 59:285–289 PubMed DOI PMC

Nagata Y, Ohtomo R, Miyauchi K, Fukuda M, Yano K, Takagi M (1994) Cloning and sequencing of a 2,5-dichloro-2,5-cyclohexadiene-1,4-diol dehydrogenase gene involved in the degradation of gamma- hexachlorocyclohexane in Pseudomonas paucimobilis. J Bacteriol 176:3117–3125 PubMed DOI PMC

NARAP (2013) “The North American Regional Action Plan NARAP (2013) on Lindane and Other Hexachlorocyclohexane (HCH) Isomers". Commission for Environmental Cooperation

Nicolaou SA, Fast AG, Nakamaru-Ogiso E, Papoutsakis ET (2013) Overexpression of fetA (ybbL) and fetB (ybbM), encoding an iron exporter, enhances resistance to oxidative stress in Escherichia coli. Appl Environ Microbiol 79(23):7210–7219 PubMed DOI PMC

Nies D (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750 PubMed DOI

Nies DH, Nies A, Chu L, Silver S (1989) Expression and nucleotide sequence of a plasmid determined divalent cation efflux system from Alcaligenes eutrophus. Proc Natl Acad Sci USA 86:7351–7355 PubMed DOI PMC

Noguchi H, Park J, Takagi T (2006) MetaGene: prokaryotic gene finding from environmental genome shotgun sequences. Nucleic Acids Res 34:5623–5630 PubMed DOI PMC

Novak R, Braun JS, Charpentier E, Tuomanen E (1998) Penicillin tolerance genes of Streptococcus pneumoniae: the ABC-type manganese permease complex Psa. Mol Microbiol 29:1285–1296 PubMed DOI

Obayori OS, Salam LB (2010) Degradation of polycyclic aromatic hydrocarbons: role of plasmids. Sci Res Essays 5(25):4093–4106

Obayori OS, Salam LB, Oyetibo GO, Idowu M, Amund OO (2017) Biodegradation potentials of polyaromatic hydrocarbon (pyrene and phenanthrene) by Proteus mirabilis isolated from an animal charcoal polluted site. Biocatal Agric Biotechnol 12:78–84 DOI

Oregaard G, Sorensen SJ (2007) High diversity of bacterial mercuric reductase genes from surface and subsurface floodplain soil (Oak Ridge, USA). ISME J 1:453–467 PubMed DOI

Osman OA, Gudasz C, Bertilsson S (2014) Diversity and abundance of aromatic genes in lake sediments in response to temperature change. FEMS Microbiol Ecol 88:468–81 PubMed DOI

Outten FW, Huffman DL, Hale JA, O’Halloran TV (2001) The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J Biol Chem 276(33):30670–30677 PubMed DOI

Pal C, Asiani K, Arya S, Rensing C, Stekel DJ, Larsson DGJ, Hobman JL (2017) Metal resistance and its association with antibiotic resistance. Adv Microb Physiol 70:261–313 PubMed DOI

Pal C, Bengtsson-Palme J, Rensing C, Kristiansson E, Larsson DG (2014) BacMet: antibacterial biocide and metal resistance genes database. Nucleic Acids Res 42(Database issue):D737–D743

Patzer SI, Hantke K (1998) The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 28(6):1199–1210 PubMed DOI

Peng Y, Leung HC, Yiu SM, Chin FY (2012) IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28:1420–1428 PubMed DOI

Pi H, Helmann JD (2017) Ferrous iron efflux systems in bacteria. Metallomics 9(7):840–851 PubMed DOI

Popp N, Schlomann M, Margit M (2006) Bacterial diversity in the active stage of a bioremediation system for mineral oil hydrocarbon-contaminated soils. Microbiology 152:3291–3304 PubMed DOI

Rather LJ, Knapp B, Haehnel W, Fuchs G (2010) Coenzyme A-dependent aerobic metabolism of benzoate via epoxide formation. J Biol Chem 285(27):P20615-20624 DOI

Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27:197–213 PubMed DOI

Salam LB (2020) Unravelling the antibiotic and heavy metal resistome of a chronically polluted soil. 3 Biotech 10(6):1-23

Salam LB (2022) Metagenomic insights into the adaptive responses of the microbiome of a spent engine oil-perturbed agricultural soil to iron stress. Geomicrobiol J. https://doi.org/10.1080/01490451.2022.2158253 DOI

Salam LB, Idris H (2019) Consequences of crude oil contamination on the structure and function of autochthonous microbial community of a tropical agricultural soil. Environ Sustain 2:167–187 DOI

Salam LB, Ilori MO, Amund OO, LiiMien Y, Nojiri H (2018) Characterization of bacterial community structure in a hydrocarbon-contaminated tropical African soil. Environ Technol 39(7):939–951 PubMed DOI

Salam LB, Obayori OS (2014) Fluorene biodegradation potentials of Bacillus strains isolated from tropical hydrocarbon-contaminated soils. Afr J Biotechnol 13(14):1554–1559 DOI

Salam LB, Obayori OS (2020) Remarkable shift in structural and functional properties of an animal charcoal-polluted soil accentuated by inorganic nutrient amendment. J Genet Eng Biotechnol 18:70 PubMed DOI PMC

Salam LB, Obayori OS, Ilori MO, Amund OO (2020) Effects of cadmium perturbation on the microbial community structure and heavy metal resistome of a tropical agricultural soil. Bioresour Bioprocess 7:25 DOI

Salam LB, Obayori OS, Ilori MO, Amund OO (2021) Acenaphthene biodegradation and structural and functional metagenomics of the microbial community of an acenaphthene-enriched animal charcoal polluted soil. Biocatal Agric Biotechnol 32:101951 DOI

Salam LB, Obayori SO, Nwaokorie FO, Suleiman A, Mustapha R (2017) Metagenomic insights into effects of spent engine oil perturbation on the microbial community composition and function in a tropical agricultural soil. Environ Sci Pollut Res 24:7139–7159 DOI

Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied Environ Microbiol 75:7537–7541 DOI

Schühle K, Jahn M, Ghisla S, Fuchs G (2001) Two similar gene clusters coding for enzymes of a new type of aerobic 2-aminobenzoate (anthranilate) metabolism in the bacterium Azoarcus evansii. J Bacteriol 183:5268–5278 PubMed DOI PMC

Sei K, Inoue D, Wada K et al (2004) Monitoring behaviour of catabolic genes and change of microbial community structures in seawater microcosms during aromatic compound degradation. Water Res 38:4405–14 PubMed DOI

Seo J-S, Keum Y-S, Li QX (2009) Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 6:278–309 PubMed DOI PMC

Singh SN, Kumari B, Upadhyay SK et al (2013) Bacterial degradation of pyrene in minimal salt medium mediated by catechol dioxygenases: enzyme purification and molecular size determination. Bioresour Technol 133:293–300 PubMed DOI

Smith CB, Johnson CN, King GM (2012) Assessment of polyaromatic hydrocarbon degradation by a potentially pathogenic environmental Vibrio parahaemolyticus isolates from coastal Louisiana, USA. Mar Pollut Bull 64(1):138–143 PubMed DOI

Sobota JM, Imlay JA (2011) Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese. Proc Natl Acad Sci USA 108(21402925):5402–5407 PubMed DOI PMC

Stay FS, Katko A, Rohm CM, Feix MA, Larsen DP (1988) Effects of fluorene on microcosms developed from natural communities. Environ Toxicol Chem 7:635–644 DOI

Táncsics A, Szabó I, Baka E et al (2010) Investigation of catechol 2,3-dioxygenase and 16S rRNA gene diversity in hypoxic, petroleum hydrocarbon contaminated groundwater. Syst Appl Microbiol 33:398–406 PubMed DOI

Thomas P, Wofford HW, Neff JM (1981) Biochemical stress responses of striped mullet (Mugil cephalus) to fluorene analog. Aquatic Toxicol 1:329–342 DOI

Trenz SP, Engesser KH, Fischer P, Knackmuss HJ (1994) Degradation of fluorene by Brevibacterium sp. strain DPO 1361: a novel C-C bond cleavage mechanism via 1, 10-dihydro-1, 10-dihydroxyfluorene-9-one. J Bacteriol 176:789–795 PubMed DOI PMC

Valderrama JA, Durante-Rodríguez G, Blázquez B, García JL, Carmona M, Díaz E (2012) Bacterial degradation of benzoate: cross-regulation between aerobic and anaerobic pathways. J Biol Chem 287(13):10494–10508 PubMed DOI PMC

Vasilieva S, Tanirbergenov B, Abilev S, Migatchev G, Huttunen MT (1990) A comparative study of mutagenic and SOS-inducing activity of biphenyls, phenanthrene-quinones, and fluorenones. Mutat Res 244:321–330 PubMed DOI

von der Weid I, Marques JM, Cunha CD et al (2007) Identification and biodegradation potential of a novel strain of Dietzia cinnamea isolated from a petroleum-contaminated tropical soil. Syst Appl Microbiol 30(4):331–339 PubMed DOI

Wang PP, Sun GX, Zhu YG (2014) Identification and characterization of arsenite methyltransferase from an archaeon Methanosarcina acetivorans C2A. Environ Sci Technol 48:12706–12713 PubMed DOI

Wang XB, Chi CQ, Nie Y et al (2011) Degradation of petroleum hydrocarbons (C6–C40) and crude oil by a novel Dietzia strain. Bioresour Technol 102(17):7755–7761 PubMed DOI

Ward SK, Abomoelak B, Hoye EA, Steinberg H, Talaat AM (2010) CtpV: a putative copper exporter required for full virulence in Mycobacterium tuberculosis. Mol Microbiol 77:1096–1110 PubMed DOI PMC

Wattiau P, Bastiaens L, van Herwijnen R et al (2001) Fluorene degradation by Sphingomonas sp. LB126 proceeds through protocatechuic acid: a genetic analysis. Res Microbiol 152:861–872 PubMed DOI

WHO (2014) World Health Organization "Lindane in Drinking Water: Background Document for Development of WHO Guidelines for Drinking-Water Quality"

Winderl C, Schaefer S, Lueders T (2007) Detection of anaerobic toluene and hydrocarbon degraders in contaminated aquifers using benzylsuccinate synthase (bssA) genes as a functional marker. Environ Microbiol 9:1035–46 PubMed DOI

Wu P, Wang Y-S (2021) Fluorene degradation by Rhodococcus sp. A2–3 isolated from hydrocarbon contaminated sediment of the Pearl River estuary. China. Ecotoxicology 30:929–935 PubMed DOI

Yadid I, Rudolph J, Hlouchova K, Copley SD (2013) Sequestration of a highly reactive intermediate in an evolving pathway for degradation of pentachlorophenol. Proc Natl Acad Sci USA 110:E2182–E2190 PubMed DOI PMC

Yang S, Wen X, Zhao L, Shi Y, Jin H (2014) Crude oil treatment leads to shift of bacterial communities in soils from the deep active layer and upper permafrost along the China-Russia Crude Oil Pipeline route. PloS One 9(5):e96552 PubMed DOI PMC

Zhang D-C, Mörtelmaier C, Margesin R (2012) Characterization of the bacterial archaeal diversity in hydrocarbon-contaminated soil. Sci Total Environ 421–422:184–196 PubMed DOI

Zhuang L, Tang Z, Ma J, Yu Z, Wang Y, Tang J (2019) Enhanced anaerobic biodegradation of benzoate under sulfate-reducing conditions with conductive iron-oxides in sediment of Pearl River estuary. Front Microbiol 10:374 PubMed DOI PMC