Table 2.

Heavy metal resistome detected in 3S metagenome (using BacMet) involved in resistance to heavy metals

Heavy metal	Enzymes/gene	Taxonomic affiliation
Copper, zinc, silver Iron, zinc, cobalt, nickel, copper, cadmium, Manganese, gallium	Copper resistance D; apolipoprotein N-acyltransferase actA (Cu/Zn); copper translocating P-type ATPase copB; cutE gene product; multicopper oxidase type 2 cutO; RND efflux system, inner membrane protein cmeB (Cu/Co); heavy metal translocating P-type ATPase copA; copper resistance protein copC; CopS protein; winged helix family two component heavy metal response transcriptional regulator copR; copper-sensing transcriptional repressor csoR; copper-translocating P-type ATPase cueA; MerR family transcriptional regulator cueR; metal-transporting P-type ATPase cueA (Cu/Ag); CutA1 divalent ion tolerance protein cutA; copper-binding protein cinA; RND efflux system, outer membrane protein cmeC (Cu/Co); multicopper oxidase type 3 cutO; molecular chaperone dnaK; transcriptional regulator copY; Cu(I)-responsive transcriptional regulator hmrR (Cu/HCl); Copper homeostasis protein cutC; Copper resistance protein L copL; laccase cueO; metal cation transporter P-type ATPase ctpV; heavy metal-translocating P-type ATPase actP; cation efflux system protein CusA; HAE1 family transporter acrD (Cu/Zn); sensor kinase cusS (Cu/Ag); thiol:disulphide interchange protein dsbC; integral membrane sensor signal transduction histidine kinase baeS (Cu/Zn/W); heavy metal translocating P-type ATPase golT (Cu/Au); response regulator crdR; type IIS restriction enzyme R protein crdS; copper resistance protein oxidase pcoA (plasmid); heavy metal sensor kinase pcoS (plasmid); CopJ protein (plasmid); heavy metal translocating P-type ATPase copZ; cation efflux system protein cusB (plasmid); winged helix family two component transcriptional regulator baeR (Cu/Zn/W); Heavy metal-translocating P-type ATPase Cd/Co/Hg/Pb/Zn-transporting ctpG (Cu); sensor histidine kinase corS; copper exporting ATPase copP; transcriptional regulator yfmP; crdB gene Zinc/iron ZIP family permease zupT (Zn/Fe/Co/Ni/Cu/Cd); iron-dependent repressor DxtR ideR; aconitase acn (Fe); transcriptional regulatory protein basR/pmrA (Fe); ferritin pfr (Fe/Cu/Mn); iron (III) ABC transporter, ATP binding protein fbpC (Fe/Ga); TonB-dependent siderophore receptor fpvA (Mn/Fe/Co/Zn/Ni/Cu/Cd/Ga); ABC transporter family protein ybtQ (Fe); cation efflux family protein fieF (Fe/Zn/Co/Cd/Ni); Fe2+/Zn2+/Mn2+ ABC transporter ATP-binding protein troB; iron chelate ABC transporter, ATP-binding protein yfeB (Fe/Mn); Fe3+ ABC superfamily ATP-binding cassette transporter, permease protein fbpB (Fe/Ga); manganese transport protein mntH (Mn/Fe/Cd/Co/Zn); permease and ATP-binding protein of yersiniabactin-iron ABC transporter ybtP (Fe); Mn2+/ Fe2+ transporter NRAMP family (mntH/yfeB); TonB-dependent siderophore receptor fptA (Fe/Co/Ni/Ga); ferric uptake regulator family protein furA (Fe); cation-activated repressor protein troR (Zn/Mn/Fe); Fe2+/Zn2+/Mn2+ ABC transporter membrane protein troD; ferritin Dps family protein dpsA (Fe/H2O2); chealated iron ABC transporter, permease yfeC (Fe/Mn); bacterioferritin bfrA (Fe); periplasmic iron-binding protein yfeA (Fe/Mn); putative ABC transport system permease fetB (Fe); iron transport inner membrane protein sitC (plasmid) (Fe/Mn/H2O2); fur regulated iron transporter sitB (plasmid) (Fe/Mn/H2O2); ferroxidase pfr (Fe/Cu/Mn); Chain A, Periplasmic Zinc Binding Protein troA (Zn/Mn/Fe); cation transport P-type ATPase nia (plasmid) (Fe/Ni)	Rhodopseudomonas palustris BisB18; alphaproteobacterium BAL199; Methylobacterium sp. 4–46; Acidithiobacillus ferrooxidans ATCC 53993; Xenorhabdus bovienii SS-2004; Starkeya novella DSM 506; Campylobacter coli JV20; Paenibacillus dendritiformis C454; Thermobacillus composti KWC4; Ralstonia metallidurans CH34; Ralstonia pickettii 12J; Clostridium sp. M62/1; Pseudomonas syringae pv. Tomato NCPPB 1108; Pseudomonas mendocina ymp; Pseudomonas stutzeri A1501; Dickeya didantii Ech586; Marinobacter sp. Mn17-9; Campylobacter upsaliensis JV21; Streptomyces griseus XylebKG-1; Corynebacterium resistens DSM 45100; Oenococcus oeni ATCC BAA-1163; Pseudovibrio sp. JE062; Yersinia mollaretii ATCC 43969; Xanthomonas vesicatoria ATCC 35937; Aeromonas hydrophila; Mycobacterium marinum M; Beijerinckia indica subsp. indica ATCC 9039; Citrobacter youngae ATCC 29220; Pantoea stewartii subsp. stewartii DC283; Escherichia sp. TW09308; Enterococcus hirae; Photobacterium leiognathi subsp. mandapamensis svers.1.1; Glaciecola sp. 4H-3-7+YE-5; Agrobacterium tumefaciens F2; Helicobacter pylori 35A; Salmonella enterica ser.. Typhimurium; Helicobacter pylori 2017; Serratia marcescens; Ralstonia metallidurans CH34; Paenibacillus elgii B69; Escherichia coli STEC_DG131-3; Stenotrophomonas maltophilia R551-3; Saccharomonospora viridis DSM 43017; Myxococcus xanthus DK 1622; Streptococcus sp. C150; Bacillus pumilus SAFR-032 Methanosaeta harundinacea 6Ac; Corynebacterium accolens ATCC 49725; Corynebacterium nuruki S6-4; Pantoea vagans C9-1; Vibrio fischeri MJ11; Pseudomonas mendocina NK-1; Escherichia coli DEC10F; Shewanella benthica KT99; Treponema paraluiscuniculi Cuniculi A; Providencia rettgeri DSM 1131; Aggregatibacter segnis ATCC 33393; Pantoea sp. SL1_M5; Ralstonia solanacearum CFBP2957; Rhodobacter sp. SW2; Mycobacterium gilvum PYR-GCK; Treponema pallidum subsp. pallidum str. Nichols; Thioalkalimicrobium cyclium ALM1; Actinobacillus minor NM305; Rhodococcus pyridinivorans AK37; Pasteurella multocida 36950; Enterobacter cloacae subsp. cloacae ATCC 13047; Salmonella bongori NCTC 12419; Citrobacter rodentium ICC168; Cyanothece sp. PCC 7425; Treponema pallidum; Sinorhizobium meliloti 1021
Zinc, cadmium, tellurium, tungsten, cobalt, chromium nickel, manganese	BaeS gene product (Zn/W); Zn/Cd/Hg/Pb-transporting ATPase zntA (Zn/Pb/Cd); DNA-binding response regulator irlR (Cd/Zn); winged helix two component transcriptional regulator baeR (Zn/W); inorganic phosphate transporter pitA (Zn/Te); integral membrane sensor signal transduction histidine kinase actS (Cd/Zn/HCl); acriflavin resistance protein mdtB (Zn); zinc transporter zitB; high-affinity zinc transporter ATPase znuC (Zn); Zn(II)-responsive transcriptional regulator zntR; multidrug resistance transporter mdrL (Zn/Co/Cr); probable RND efflux transporter mdtB (Zn); membrane fusion protein (MFP-RND) heavy metal cation tricomponent efflux zneB/hmxB (plasmid) (Zn); high-affinity zinc transporter periplasmic component znuA (Zn); sensor protein zraS (Zn/Pb); zinc/iron permease zipB (Cd/Zn); heavy metal-translocating P-type ATPase ctpC (Mn/Zn); zinc efflux system zitB (Zn); outer membrane efflux protein czcC (plasmid; Cd/Zn/Co); cation transporting ATPase, P-type ziaA (Zn); response regulator receiver protein actR (Cd/Zn/HCl); RND family efflux transporter MFP subunit 1 mdtA (Zn); transcriptional regulator zur (Zn); thiol:disulfide interchange protein dsbA (Cd/Zn/Hg); transcriptional regulatory protein zraR (Zn); AcrB/AcrD/AcrF family protein nczA (Ni/Co/Zn); RND divalent metal cation efflux transporter czrA (Zn/Cd); cadmium-zinc-nickel resistance protein cznA (Cd/Zn/Ni); cadmium-translocating P-type ATPase czcP (Cd/Zn/Co); heavy metal response regulator irlR (Cd/Zn); dsbA-like protein frnE (Cd/H2O2); twin-arginine translocation pathway signal mntA (Cd/Mn); MerR family transcriptional regulator cadR (plasmid, Cd)	Edwardsiella tarda EIB202; Pectobacterium carotovorum subsp. brasiliensis PBR1692; Burkholderia oklahomensis EO147; Geobacter sp. M18; Achromobacter piechaudii ATCC 43553; Sinorhizobium meliloti CCNWSX0020; Ralstonia pickettii 12J; Salmonella bongori NCTC 12419; Yokenella regensburgei ATCC 43003; Edwardsiella tarda ATCC 23685; Listeria monocytogenes J0161; Pseudomonas aeruginosa NCMG1179; Cupriavidus metallidurans CH34; Plautia stali symbiont; Escherichia coli IAI39; Pseudomonas sp. TJI-51; Kineococcus radiotolerans SRS30216; Pantoea stewartii subsp. stewartii DC283; Pyrococcus abyssi GE5; Rhizobium sp. PDO-076; Achromobacter arsenitoxydans SY8; Methylococcus capsulatus str. Bath; Aggregatibacter segnis ATCC 33393; Klebsiella pneumoniae 342; Caulobacter crescentus CB15; Pseudomonas aeruginosa PA7; Helicobacter mustelae 12198; Alicycliphilus denitrificans BC; Dermacoccus sp. Ellin185; Silicibacter sp. TrichCH4B; Pseudomonas putida S16
Chromium, tellurium, selenium, molybdenum, vanadium, tungsten	ATP-dependent DNA helicase recG (Cr/Te/Se); Cr (VI) reductase (Cr, Fe, H2O2); NADPH-dependent FMN reductase chrR (Cr); putative NADH-dependent reductase yieF (Cr/V/Mo); malate dehydrogenase ruvB (Cr); chromate transporter chrA; nitroreductase A nfsA (Cr); NAD(P)H dehydrogenase (quinone) chrR (Cr); chromate resistance signal peptide protein chrB; Holliday junction DNA helicase ruvB (Cr/Te/Se); manganese/iron superoxide dismutase chrC (Cr); tellurite resistance protein tehB; tellurite resistance protein tehA; tellurite resistance protein trgB (Te/Cu); symporter actP (Te); KlaC protein klaC/telB (plasmid) (Te); molybdate ABC transporter inner membrane subunit modB (W/Mo); molybdate ABC transporter periplasmic protein wtpA (W/Mo); molybdenum ABC transporter ATP-binding protein modC (W/Mo); DNA-binding transcriptional regulator ModE (W/Mo); molybdenum ABC transporter periplasmic molybdate-binding protein modA (W/Mo); tungstate ABC transporter binding protein wtpA (W/Mo); ABC transporter, ATP-binding protein wtpC (W/Mo); molybdate/tungstate transport system permease protein wtpB; molybdenum-pterin binding domain protein/site-specific recombinase, phage integrase family tunR (W/Mo); sodA gene product (Se/H2O2); superoxide dismutase sodB (Se/H2O2)	Tolumonas auensis DSM 9187; Lysinibacillus fusiformis ZC1; Burkholderia multivorans ATCC 17616; Burkholderia cepacia; Shewanella frigidimarina NCIMB 400; Sinorhizobium meliloti BL225C; Vibrio vulnificus YJ016; Rhodobacter capsulatus SB 1003; Acinetobacter oleivorans DR1; Alkalilimnicola erhlichii MLHE-1; Alicycliphilus denitrificans K601; Haemophilus pittmaniae HK 85; Haemophilus haemolyticus M21621; Maritimibacter alkaliphilus HTCC2654; Magnetospirillum magneticum AMB-1; Ralstonia pickettii 12J; Desulfotomaculum kuznetsovii DSM 6115; Gillisia limnaea DSM 15749; Salmonella enterica subsp. enterica serovar Typhimurium str. T000240; Desulfotomaculum acetoxidans DSM 771; Methanolinea tarda NOBI-1; Thermococcus sibiricus MM 739; Thermococcus litoralis DSM 5473; Desulfovibrio vulgaris str. Hildenborough; Serratia symbiotica str. ‘Cinara cedri’; Burkholderia pseudomallei 1655
Nickel, cobalt, manganese, magnesium	Major facilitator transporter nrsD/nreB (Ni/Co); P-ATPase superfamily, P-type ATPase cadmium transporter ctpD (Co/Ni); cation transporter dmeF (Co/Ni); magnesium and cobalt transport protein corA (Mg/Co/Ni); nickel ABC transporter substrate-binding protein nikA (Ni); iron-dicitrate transporter subunit, membrane component of ABC superfamily fecD (Ni/Co); nickel and cobalt resistance protein cnrA (Co/Ni); nickel transporter ATP-binding protein nikE (Ni); nickel ABC superfamily ATP binding cassette transporter, ABC protein nikD (Ni); integral membrane sensor signal transduction histidine kinase nrsS (Ni); high-affinity nickel transporter rcnA (Ni/Co/Fe); fecE gene product (Ni/Co); periplasmic nickel sensor cnrR/cnrX (plasmid, Ni); RNA polymerase sigma factor cnrH (plasmid, Co/Ni); nickel ABC transporter, permease subunit nikC (Ni); transcriptional regulator, copG family protein nikR (Ni); nickel ABC transporter permease nikB; czcA family heavy metal efflux pump nrsA (Ni); nickel/cobalt efflux system ncrC (Co/Ni); RNA polymerase sigma factor nccH (plasmid; Ni/Co/Cd); ArsR family transcriptional regulator cmtR (Co/Ni); conserved inner membrane protein mntP (Mn/Mg); magnesium-transporting ATPase P-type 1 mgtA; CO2+/Mg2+ efflux protein ApaG corD (Co/Mg); magnesium and cobalt efflux protein corB; Mg/Co transporter corC; magnesium/nickel/cobalt transporter corA	Roseiflexus sp. RS-1; Mycobacterium parascrofulaceum ATCC BAA-614; Pelobacter carbinolicus DSM 2380; Alkanivorax sp. DG881; Dickeya dadantii Ech703; Escherichia coli S88; Bradyrhizobium sp. STM 3843; Rhodospirillum rubrum ATCC 11170; Roseomonas cervicalis ATCC 49957; Cyanothece PCC 7424; Starkeya novella DSM 506; Xenorhabdus nematophila ATCC 19061; Cupriavidus metallidurans CH34; Brucella sp. NF 2653; Sagittula stellata E-37; Desulfotomaculum kuznetsovii DSM 6115; Klebsiella oxytoca 10-5245; Clavibacter michiganensis subsp. sepedonicus; Pantoea stewartii subsp. stewartii DC283; Klebsiella oxytoca 10-5246; Pseudomonas psychrotolerans L19; Vibrio sp. Ex25; Idiomarina loihensis L2TR; Actinobacillus succinogenes 130Z
Mercury, lead, arsenic, antimony	Mercuric reductase merA; periplasmic mercury transport protein merT; alkylmercury lyase merB2; MerR family transcriptional regulator merR1; heavy metal transport/detoxification protein merP; copper-transporting ATPase merT-P; putative mercury transport protein merC (plasmid); Pb-efflux ATPase pbrA; Pb-specific transcription regulator protein pbrR (plasmid); iron permease FTR1 family protein 2 pbrT (plasmid); phosphate import ATP binding protein pstB (As); arsenical resistance protein arsB (As); arsenical resistance protein acr3 (As); arsenite efflux pump ACR3 arsB (As/Sb); arsenate reductase arsC (As/Sb); molydopterin dinucleotide binding region (As); methyltransferase type 11 arsM; phosphate-binding protein pstS (As); phosphate ABC transporter permease protein pstC (As); MIP family channel protein glpF (As/Sb); phosphate transporter permease subunit A pstA (As); arsenical pump-driving ATPase arsA (plasmid, As/Sb); putative arsenic-efflux pump regulatory protein arsR (As/Sb/Bi); putative sensor histidine kinase aioS/aoxS (As); arsenite oxidase small subunit (As); arsenite oxidase large subunit	Micromonospora sp. L5; Thiobacillus sp.; Nocardioides sp. JS614; Xanthobacter autotrophicus Py2; Croceibacter atlanticus HTCC2559; Acidithiobacillus ferrooxidans ATCC 53993; Ralstonia metallidurans CH34; Herbaspirillum seropedicae SmR1; Achromobacter xylosoxidans A8; Sutterella wadsworthensis 3_1_45B; Moorella thermoacetica ATCC 39073; Campylobacter lari; Synechococcus sp. PCC 7002; Lactobacillus reuteri SD2112; Pyrobaculum calidifontis JCM 11548; Intrasporangium calvum DSM 43043; Cupriavidus basiliensis OR16; Nitrococcus mobilis Nb-231; Pseudomonas fulva 12-X; Leptothrix cholodnii SP-6; Klebsiella pneumoniae 342; Agrobacterium tumefaciens; Burkholderia multivorans ATCC 17616; Roseovarius sp. 217