Environmental microorganisms usually exhibit a high level of genomic plasticity and metabolic versatility that allow them to be well-adapted to diverse environmental challenges. This study used shotgun metagenomics to decipher the functional and metabolic attributes of an uncultured Paracoccus recovered from a polluted soil metagenome and determine whether the detected attributes are influenced by the nature of the polluted soil. Functional and metabolic attributes of the uncultured Paracoccus were elucidated via functional annotation of the open reading frames (ORFs) of its contig. Functional tools deployed for the analysis include KEGG, KEGG KofamKOALA, Clusters of Orthologous Groups of proteins (COG), Comprehensive Antibiotic Resistance Database (CARD), and the Antibiotic Resistance Gene-ANNOTation (ARG-ANNOT V6) for antibiotic resistance genes, TnCentral for transposable element, Transporter Classification Database (TCDB) for transporter genes, and FunRich for gene enrichment analysis. Analyses revealed the preponderance of ABC transporter genes responsible for the transport of oligosaccharides (malK, msmX, msmK, lacK, smoK, aglK, togA, thuK, treV, msiK), monosaccharides (glcV, malK, rbsC, rbsA, araG, ytfR, mglA), amino acids (thiQ, ynjD, thiZ, glnQ, gluA, gltL, peb1C, artP, aotP, bgtA, artQ, artR), and several others. Also detected are transporter genes for inorganic/organic nutrients like phosphate/phosphonate, nitrate/nitrite/cyanate, sulfate/sulfonate, bicarbonate, and heavy metals such as nickel/cobalt, molybdate/tungstate, and iron, among others. Antibiotic resistance genes that mediate efflux, inactivation, and target protection were detected, while transposable elements carrying resistance phenotypes for antibiotics and heavy metals were also annotated. The findings from this study have established the resilience, adaptability, and survivability of the uncultured Paracoccus in the hydrocarbon-polluted soil.

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

Department of Microbiology Lagos State University Ojo Lagos Nigeria

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Abskharon RNN, Hassan SHA, Kabir MH, Qadir SA, Gad El Rab SM, Wang MH (2010) The role of antioxidants enzymes of E. coli ASU3, a tolerant strain to heavy metals toxicity, in combating oxidative stress of copper. World J Microbiol Biotechnol 26(2):241–247

Alfano M, Cavazza C (2020) Structure, function, and biosynthesis of nickel-dependent enzymes. Protein Sci 29(5):1071–1089 PubMed DOI PMC

Andrew RWJ, Jackson JM (1996) Pollution and waste management. The natural environment and human impact. Longman Publishers, Singapore, pp 281–297

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

Antonelli A, D’Andrea MM, Brenciani A, Galeotti CL, Morroni G, Pollini S, Varaldo PE, Rossolini GM (2018) Characterization of poxtA, a novel phenicol-oxazolidinone-tetracycline resistance gene from an MRSA of clinical origin. J Antimicrob Chemother 73(7):1763–1769 PubMed DOI

Antony R, Sujith PP, Fernandes SO, Verma P, Khedekar VD, Loka Bharathi PA (2011) Cobalt immobilization by manganese oxidizing bacteria from the Indian Ridge System. Curr Microbiol 62(3):840–849 PubMed DOI

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

Bader GD, Hogue CW (2003) An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics 4:2 PubMed DOI PMC

Bhandal IS, Hauptman RM, Widholm JM (1985) Trehalose as cryoprotectant for the freeze preservation of carrot and tobacco cells. Plant Physiol 78:430–432 PubMed DOI PMC

Bissonnette L, Roy PH (1992) Characterization of In0 of Pseudomonas aeruginosa plasmid pVS1, an ancestor of integrons of multi-resistance plasmids and transposons of gram-negative bacteria. J Bacteriol 174(4):1248–1257 PubMed DOI PMC

Bockwoldt JA, Zimmermann M, Tiso T, Blank LM (2020) Complete genome sequence and annotation of the Paracoccus pantotrophus type strain DSM 2944. Microbiol Resour Announc 9:1–2 DOI

Bonhivers M, Ghazi A, Boulanger P, Letellier L (1996) FhuA, a transporter of the Escherichia coli outer membrane, is converted into a channel upon binding of bacteriophage T5. EMBO J 15(8):1850–1856 PubMed DOI PMC

Bonnin RA, Nordmann P, Carattoli A, Poirel L (2013) Comparative genomics of IncL/M-type plasmids: evolution by acquisition of resistance genes and insertion sequences. Antimicrob Agents Chemother 57(1):674–676 PubMed DOI PMC

Bougouffa S, Radovanovic A, Essack M, Bajic VB (2014) DEOP: a database on osmoprotectants and associated pathways. Database 2014

Cai J, Wang Y, Schwarz S et al (2015) Enterococcal isolates carrying the novel oxazolidinone resistance gene optrA from hospitals in Zhejiang, Guangdong, and Henan, China, 2010–2014. Clin Microbiol Infect 21(12):1095-e1 DOI

Carmel G, Coulton JW (1991) Internal deletions in the FhuA receptor of Escherichia coli K-12 define domains of ligand interactions. J Bacteriol 173(14):4394–4403 PubMed DOI PMC

Caza M, Kronstad JW (2013) Shared and distinct mechanisms of iron acquisition by bacterial and fungal pathogens of humans. Front Cell Infect Microbiol 3:80 PubMed DOI PMC

Chesneau O, Ligeret H, Hosan-Aghaie N, Morvan A, Dassa E (2005) Molecular analysis of resistance to streptogramin A compounds conferred by the Vga proteins of staphylococci. Antimicrob Agents Chemother 49(3):973–980 PubMed DOI PMC

Chouchani C, El Salabi A, Marrakchi R, Ferchichi L, Walsh TR (2012) First report of mefA and msrA/msrB multidrug efflux pumps associated with blaTEM-1 β-lactamase in Enterococcus faecalis. Int J Infect Dis 16(2):e104–e109 PubMed DOI

Cui J, Davidson AL (2011) ABC solute importers in bacteria. Essays Biochem 50:85–99 PubMed DOI

Cuthbertson L, Kos V, Whitfield C (2010) ABC transporters involved in export of cell surface glycoconjugates. Microbiol Mol Biol Rev 74:341–362 PubMed DOI PMC

Cuzon G, Naas T, Nordmann P (2011) Functional characterization of Tn4401, a Tn3-based transposon involved in blaKPC gene mobilization. Antimicrob Agents Chemother 55(11):5370–5373 PubMed DOI PMC

Dai Z, Wu Z, Zhu W, Wu G (2022) Amino acids in microbial metabolism and function. Adv Exp Med Biol 1354:127–143 PubMed DOI

Davidson AL, Dassa E, Orelle C, Chen J (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72:317–364 PubMed DOI PMC

Decewicz P, Dziewit L, Golec P, Kozlowska P, Bartosik D, Radlinska M (2019) Characterization of the virome of Paracoccus spp. (Alphaproteobacteria) by combined in silico and in vivo approaches. Sci Rep 9:7899

Deole R, Hoff WD (2020) A potassium chloride to glycine betaine osmoprotectant switch in the extreme halophile Halorhodospira halophila. Sci Rep 10:3383 PubMed DOI PMC

Elleuche S, Fodor K, von der Heyde A, Klippel B, Wilmanns M, Antranikian G (2014) Group III alcohol dehydrogenase from Pectobacterium atrosepticum: insights into enzymatic activity and organization of the metal ion-containing region. Appl Microbiol Biotechnol 98(9):4041–4051 PubMed DOI

Ero R, Kumar V, Su W, Gao YG (2019) Ribosome protection by ABC-F proteins - molecular mechanism and potential drug design. Protein Sci 28(4):684–693 PubMed DOI PMC

Fernandez JE, Perreten V, Schwendener S (2021) The novel macrolide resistance genes mef(F) and msr(G) are located on a plasmid in Macrococcus canis and a transposon in Macrococcus caseolyticus. J Antimicrob Chemother 76(1):48–54 PubMed DOI

Galinski EA, Herzog RM (1990) The role of trehalose as a substitute for nitrogen-containing compatible solutes (Ectothiorhodospira halochloris). Arch Microbiol 153:607–613 DOI

Greene NP, Kaplan E, Crow A, Koronakis V (2018) Antibiotic resistance mediated by the MacB ABC transporter family: a structural and functional perspective. Front Microbiol 9:950 PubMed DOI PMC

Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L, Rolain JM (2014) ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 58:212–220 PubMed DOI PMC

Hoffmann T, Bremer E (2017) Guardians in a stressful world: the Opu family of compatible solute transporters from Bacillus subtilis. Biol Chem 398:193–214 PubMed DOI

Hottiger T, Boller T, Wiemken A (1989) Correlation of trehalose content and heat resistance in yeast mutants altered in the RAS/adenylate cyclase pathway: is trehalose a thermoprotectant. FEBS Lett 255:431–434 PubMed DOI

Huda N, Lee EW, Chen J, Morita Y, Kuroda T, Mizushima T, Tsuchiya T (2003) Molecular cloning and characterization of an ABC multidrug efflux pump, VcaM, in non-O1 Vibrio cholerae. Antimicrob Agents Chemother 47(8):2413–2417 PubMed DOI PMC

Jung YH, Shin ES, Kim O, Yoo JS, Lee KM, Yoo JI, Chung GT, Lee YS (2010) Characterization of two newly identified genes, vgaD and vatH, [corrected] conferring resistance to streptogramin A in Enterococcus faecium. Antimicrob Agents Chemother 54(11):4744–4749 PubMed DOI PMC

Kalaiyezhini D, Ramachandran KB (2015) Biosynthesis of poly-3-hydroxybutyrate (PHB) from glycerol by Paracoccus denitrificans in a batch bioreactor: effect of process variables. Prep Biochem Biotechnol 45:69–83 PubMed DOI

Kerr ID, Reynolds ED, Cove JH (2005) ABC proteins and antibiotic drug resistance: is it all about transport. Biochem Soc Trans 33:1000–1002 PubMed DOI

Kletzin A, Adams MWW (1996) Tungsten in biological systems. FEMS Microbiol Rev 18:5–63 PubMed DOI

Kohl M, Wiese S, Warscheid B (2011) Cytoscape: software for visualization and analysis of biological networks. Methods Mol Biol 696:291–303 PubMed DOI

Kun-Tai L, Dong-Hong L, Ying-Ping Z, Yong-Hong W, Ju C, Si-Liang Z (2008) Influence of Zn DOI

Lavilla Lerma L, Benomar N, Valenzuela AS, Casado Muñoz Mdel C, Gálvez A, Abriouel H (2014) Role of EfrAB efflux pump in biocide tolerance and antibiotic resistance of Enterococcus faecalis and Enterococcus faecium isolated from traditional fermented foods and the effect of EDTA as EfrAB inhibitor. Food Microbiol 44:249–257 PubMed DOI

Lenart J, Vimberg V, Vesela L, Janata J, Balikova Novotna G (2015) Detailed mutational analysis of Vga(A) interdomain linker: implication for antibiotic resistance specificity and mechanism. Antimicrob Agents Chemother 59:1360–1364 PubMed DOI PMC

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

Locher KP (2016) Mechanistic diversity in ATP-binding cassette (ABC) transporters. Nat Struct Mol Biol 23:487–493 PubMed DOI

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

Matsuo T, Chen J, Minato Y, Ogawa W, Mizushima T, Kuroda T, Tsuchiya T (2008) SmdAB, a heterodimeric ABC-type multidrug efflux Pump, in Serratia Marcescens. J Bacteriol 190(2):648–654 PubMed DOI

McArthur AG, Waglechner N, Nizam F et al (2013) The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 57(7):3348–3357 PubMed DOI PMC

Meyer JF, Nies BA, Wiedemann BERND (1983) Amikacin resistance mediated by multi-resistance transposon Tn2424. J Bacteriol 155(2):755–760 PubMed DOI PMC

Minamihata K, Goto M, Kamiya N (2012) Activation of Pyrococcus furiosus alkaline phosphatase by divalent metal ions. Biotechnol Lett 34(11):2055–2060 PubMed DOI

Mota MJ, Lopes RP, Simões MMQ, Delgadillo I, Saraiva JA (2019) Effect of high pressure on Paracoccus denitrificans growth and Polyhydroxyalkanoates production from glycerol. Appl Biochem Biotechnol 188:810–823 PubMed DOI

Moura A, Soares M, Pereira C, Leitão N, Henriques I, Correia A (2009) INTEGRALL: a database and search engine for integrons, integrases and gene cassettes. Bioinformatics 25(8):1096–1098 PubMed DOI

Ning M, Hao W, Cao C et al (2020) Toxicity of deltamethrin to Eriocheir sinensis and the isolation of a deltamethrin-degrading bacterium, Paracoccus sp. P-2. Chemosphere 257:127162

Novotna G, Janata J (2006) A new evolutionary variant of the streptogramin A resistance protein, Vga(A)LC, from Staphylococcus haemolyticus with shifted substrate specificity towards lincosamides. Antimicrob Agents Chemother 50(12):4070–4076 PubMed DOI PMC

Obayori OS, Ilori MO, Adebusoye SA, Amund OO, Oyetibo GO (2008) Microbial population changes in tropical agricultural soil experimentally contaminated with crude petroleum. Afr J Biotechnol 7:4512–4520

Obayori OS, Salam LB, Anifowoshe WT, Odunewu ZM, Amosu OE, Ofulue BE (2015) Enhanced degradation of petroleum hydrocarbons in corn-steep-liquor-treated soil microcosm. Soil Sediment Contam 24(7):731–743 DOI

Partridge SR, Hall RM (2003) In34, a complex In5 family class 1 integron containing orf513 and dfrA10. Antimicrob Agents Chemother 47(1):342–349 PubMed DOI PMC

Pathan M, Keerthikumar S, Ang C-S et al (2015) FunRich: an open access standalone functional enrichment and interaction network analysis tool. Proteomics 15(15):2597–2601 PubMed DOI

Pau RN, Lawson DM (2002) Transport, homeostasis, regulation, and binding of molybdate and tungstate to proteins. Metal Ions Biol Syst 39:31–74

Pierce JR, Earhart CF (1986) Escherichia coli K-12 envelope proteins specifically required for ferrienterobactin uptake. J Bacteriol 166(3):930–936 PubMed DOI PMC

Poole K (2005) Efflux-mediated antimicrobial resistance. J Antimicrob Chemother 56(1):20–51 PubMed DOI

Puri A, Bajaj A, Singh Y, Lal R (2022) Harnessing taxonomically diverse and metabolically versatile genus Paracoccus for bioplastic synthesis and xenobiotic biodegradation. J Appl Microbiol 132:4208–4224 PubMed DOI

Puri A, Bajaj A, Verma H, Kumar R, Singh Y (2020) Complete genome sequence of Paracoccus sp. strain AK26: insights into multipartite genome architecture and methylotropy. Genomics 112:2572–2582 PubMed DOI

Raetz CRH, Reynolds CM, Trent MS, Bishop RE (2007) Lipid A modification systems in gram-negative bacteria. Annu Rev Biochem 76:295–329 PubMed DOI PMC

Rath H, Reder A, Hoffmann T, Hammer E, Seubert A, Bremer E, Völker U, Mäder U (2020) Management of osmoprotectant uptake hierarchy in Bacillus subtilis via a SigB-dependent antisense RNA. Front Microbiol 11:622 PubMed DOI PMC

Rho M, Tang H, Ye Y (2010) FragGeneScan: predicting genes in short and error-prone reads. Nucleic Acid Res 38:20–191 DOI

Rodionov DA, Hebbeln P, Gelfand MS, Eitinger T (2006) Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP-binding cassette transporters. J Bacteriol 188(1):317–327 PubMed DOI PMC

Ross K, Varani AM, Snesrud E et al (2021) TnCentral: a prokaryotic transposable element database and web portal for transposon analysis. MBio 12:e02060–21

Rudolph AS, Crowe JH, Crowe LM (1986) Effects of three stabilizing agents – proline, betaine. and trehalose – on membrane phospholipids. Arch Biochem Biophys 245:134–143 PubMed DOI

Ruiz N, Gronenberg LS, Kahne D, Silhavy TJ (2008) Identification of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 105:5537–5542 PubMed DOI PMC

Sahoo B, Ningthoujam R, Chaudhuri S (2018) Isolation and characterization of a lindane degrading bacteria Paracoccus sp. NITDBR1 and evaluation of its plant growth promoting traits. Int Microbiol 22:155–167 PubMed DOI

Saier Jr MH, Reddy VS, Tamang DG, Västermark A (2014) The transporter classification database. Nucleic Acids Res 42(Database issue):D251-D258

Salam LB (2018) Detection of carbohydrate-active enzymes and genes in a spent engine oil-perturbed agricultural soil. Bull Natl Res Cent 42:10 DOI

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

Salam LB, Ishaq A (2019) Biostimulation potentials of corn steep liquor in enhanced hydrocarbon degradation in chronically polluted soil. 3 Biotech 9:46

Salam LB, Obayori OS, Ilori MO, Amund OO (2021) Impact of spent engine oil contamination on the antibiotic resistome of a tropical agricultural soil. Ecotoxicology 30:1251–1271 PubMed DOI

Schwendener S, Donà V, Perreten V (2020) The novel macrolide resistance genes mef(D), msr(F), and msr(H) are present on resistance islands in Macrococcus canis, Macrococcus caseolyticus, and Staphylococcus aureus. Antimicrob Agents Chemother 64(5):e00160–e220 PubMed DOI PMC

Sharkey LK, Edwards TA, O’Neill AJ (2016) ABC-F proteins mediate antibiotic resistance through ribosomal protection. Mbio 7:e01975 PubMed DOI PMC

Shea CM, McIntosh MA (1991) Nucleotide sequence and genetic organization of the ferric enterobactin transport system: homology to other periplasmic binding protein-dependent systems in Escherichia coli. Mol Microbiol 5(6):1415–1428 PubMed DOI

Siche S, Neubauer O, Hebbeln P, Eitinger T (2010) A bipartite S unit of an ECF-type cobalt transporter. Res Microbiol 161(10):824–829 PubMed DOI

Singh KV, Malathum K, Murray BE (2001) Disruption of an Enterococcus faecium species-specific gene, a homologue of acquired macrolide resistance genes of staphylococci, is associated with an increase in macrolide susceptibility. Antimicrob Agents Chemother 45(1):263–266 PubMed DOI PMC

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

Spanning RJM, Stouthamer AH, Baker SC, Verseveld HW (2015) Paracoccus. Bergey’s manual systematic archaea bacteriology. John Wiley & Sons Inc, Hoboken, NJ, pp 1–14

Szklarczyk D, Gable AL, Nastou KC et al (2021) The STRING database in 2021: customizable protein–protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res 49:D605–D612 PubMed DOI

Tansirichaiya S, Rahman MA, Roberts AP (2019) The Transposon Registry. Mobile. DNA 10:40

Tatusov RL, Natale DA, Garkavtsev IV et al (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28 PubMed DOI PMC

Tessé S, Trueba F, Berthet N, Hot C, Chesneau O (2013) Resistance genes underlying the LS PubMed DOI PMC

Tian J, Long X, Zhang S, Qin Q, Gan L, Tian Y (2018) Screening cyhalothrin degradation strains from locust epiphytic bacteria and studying Paracoccus acridae SCU-M53 cyhalothrin degradation process. Environ Sci Pollut Res 25:11505–11515 DOI

Tsuda M, Genka H (2001) Identification and characterization of Tn4656, a novel class II transposon carrying a set of toluene-degrading genes from TOL plasmid pWW53. J Bacteriol 183(21):6215–6224 PubMed DOI PMC

Van Laere A (1989) Trehalose, reserve and/or stress metabolite. FEMS Microbiol Rev 63:201–210 DOI

Wang Y, Lv Y, Cai J et al (2015) A novel gene, optrA, that confers transferable resistance to oxazolidinones and phenicols and its presence in Enterococcus faecalis and Enterococcus faecium of human and animal origin. J Antimicrob Chemother 70(8):2182–2190 PubMed DOI

Welsh DT (2000) Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev 24(3):263–290 PubMed DOI

Welsh DT, Herbert RA (1999) Osmotically induced intracellular trehalose, but not glycine betaine accumulation promotes desiccation tolerance in Escherichia coli. FEMS Microbiol Lett 174:57–63 PubMed DOI

Wilson DN (2016) The ABC of ribosome-related antibiotic resistance. Mbio 7:e00598–e1516 PubMed DOI PMC

Wilson DN, Hauryliuk V, Atkinson GC, O’Neill AJ (2020) Target protection as a key antibiotic resistance mechanism. Nat Rev Microbiol 18(11):637–648 PubMed DOI

Wong K, Ma J, Rothnie A, Biggin PC, Kerr ID (2014) Towards understanding promiscuity in multidrug efflux pumps. Trends Biochem Sci 39:8–16 PubMed DOI

Wu Y, Fan R, Wang Y et al (2019) Analysis of combined resistance to oxazolidinones and phenicols among bacteria from dogs fed with raw meat/vegetables and the respective food items. Sci Rep 9:15500 PubMed DOI PMC

Zamble D (2017) Introduction to the biological chemistry of nickel. RSC Metallobiology 2017:1–11

Zawadzka AM, Kim Y, Maltseva N, Nichiporuk R, Fan Y, Joachimiak A, Raymond KN (2009) Characterization of a Bacillus subtilis transporter for petrobactin, an anthrax stealth siderophore. Proc Natl Acad Sci U S A 106(51):21854–21859 PubMed DOI PMC

Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214 PubMed DOI