Abstract
Marine hydrocarbonoclastic bacteria can use polycyclic aromatic hydrocarbons as carbon and energy sources, that makes these bacteria highly attractive for bioremediation in oil-polluted waters. However, genomic and metabolic differences between species are still the subject of study to understand the evolution and strategies to degrade PAHs. This study presents Rhodococcus ruber MSA14, an isolated bacterium from marine sediments in Baja California, Mexico, which exhibits adaptability to saline environments, a high level of intrinsic pyrene tolerance (> 5 g L− 1), and efficient degradation of pyrene (0.2 g L− 1) by 30% in 27 days. Additionally, this strain demonstrates versatility by using naphthalene and phenanthrene as individual carbon sources. The genome sequencing of R. ruber MSA14 revealed a genome spanning 5.45 Mbp, a plasmid of 72 kbp, and three putative megaplasmids, lengths between 110 and 470 Kbp. The bioinformatics analysis of the R. ruber MSA14 genome revealed 56 genes that encode enzymes involved in the peripheral and central pathways of aromatic hydrocarbon catabolism, alkane, alkene, and polymer degradation. Within its genome, R. ruber MSA14 possesses genes responsible for salt tolerance and siderophore production. In addition, the genomic analysis of R. ruber MSA14 against 13 reference genomes revealed that all compared strains have at least one gene involved in the alkanes and catechol degradation pathway. Overall, physiological assays and genomic analysis suggest that R. ruber MSA14 is a new haloalkalitolerant and hydrocarbonoclastic strain toward a wide range of hydrocarbons, making it a promising candidate for in-depth characterization studies and bioremediation processes as part of a synthetic microbial consortium, as well as having a better understanding of the catabolic potential and functional diversity among the Rhodococci group.
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Data availability
The genome sequences were deposited in the GenBank of the National Center for Biotechnology Information (NCBI) database under the BioProject accession number PRJNA944780 and Biosample SAMN33761289. The chromosome accession number is CP145319, and the assigned accession numbers of the putative plasmids are CP145320, CP145321, CP145322, and CP145323. SRA files (Sequence Read Archive) containing the raw data assigned the accession number SRR24949810.
Abbreviations
- ANOVA:
-
Analysis of variance
- ABC:
-
ATP-binding cassette
- BV:
-
Baeyer-Villiger pathway
- BGC:
-
Biosynthetic gene clusters
- BH:
-
Bushnell Haas
- CDS:
-
Coding sequences
- CFU:
-
Colony-forming unit
- Cyt:
-
Cytochrome
- E24:
-
Emulsification activity
- GC-MSD:
-
Gas chromatography-mass spectrometry detector
- HADEG:
-
Hydrocarbon Aerobic Degradation Enzymes and Genes
- HMW:
-
High molecular weight
- LMW:
-
Low molecular weight
- LB:
-
Luria Bertani
- MFS:
-
Major facilitator superfamily
- MHCB:
-
Marine hydrocarbonoclastic bacteria
- NCBI:
-
National Center for Biotechnology Information
- NRPS:
-
Non-ribosomal peptide-synthases
- OD:
-
Optical density
- OG:
-
Orthologous gene
- PEG:
-
Polyethyleneglycol
- PAHs:
-
Polycyclic aromatic hydrocarbons
- PCA:
-
Principal component analysis
- RAST:
-
Rapid Annotation using Subsystem Technology
- T1PKS:
-
Type 1 polyketide synthase
- antiSMASH:
-
Antibiotics & Secondary Metabolite Analysis SHell
References
Abdelhaleem HAR, Zein HS, Azeiz A, Sharaf AN, Abdelhadi AA (2019) Identification and characterization of novel bacterial polyaromatic hydrocarbon-degrading enzymes as potential tools for cleaning up hydrocarbon pollutants from different environmental sources. Environ Toxicol Pharmacol 67:108–116. https://doi.org/10.1016/j.etap.2019.02.009
Afordoanyi DM, Akosah YA, Shnakhova L, Saparmyradov K, Diabankana RGC, Validov S (2023) Biotechnological key genes of the Rhodococcus erythropolis MGMM8 genome: genes for bioremediation, antibiotics, plant protection, and growth stimulation. Microorganisms 12:88. https://doi.org/10.3390/microorganisms12010088
Alvarez HM (2010) Central metabolism of species of the genus Rhodococcus. In: Alvarez HM (ed) Biology of Rhodococcus, 1st edn. Springer-, Berlin, pp 91–108. https://doi.org/10.1007/978-3-642-12937-7_4
Andrews S (2010) FastQC: A Quality Control Tool for High Throughput Sequence Data. Babraham Bioinformatics. Available online: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/
Aziz RK, Bartels D, Best A, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: Rapid annotations using subsystems technology. BMC Genomics 9. https://doi.org/10.1186/1471-2164-9-75
Bagi A, Knapik K, Baussant T (2020) Abundance and diversity of n-alkane and PAH-degrading bacteria and their functional genes - potential for use in detection of marine oil pollution. Sci Total Environ 810:152238. https://doi.org/10.1016/j.scitotenv.2021.152238
Ball A, Truskewycz A (2013) Polyaromatic hydrocarbon exposure: an ecological impact ambiguity. Environ Sci Pollut Res Int 20:4311–4326. https://doi.org/10.1007/s11356-013-1620-2
Blin K, Shaw S, Augustijn HE, Reitz ZL, Biermann F, Alanjary M, Fetter A, Terlouw BR, Metcalf WW, Helfrich EJN, van Wezel GP, Medema MH, Weber T (2023) antiSMASH 7.0: new and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Res 51:W46–W50. https://doi.org/10.1093/nar/gkad344
Cafaro V, Izzo V, Notomista E, Di Donato A (2013) Marine hydrocarbonoclastic bacteria. Marine enzymes for Biocatalysis: sources, biocatalytic characteristics and bioprocesses of Marine enzymes. Elsevier Ltd., pp 373–402. https://doi.org/10.1533/9781908818355.3.373
Cantera S, Di Benedetto F, Tumulero BF, Sousa DZ (2023) Microbial conversion of carbon dioxide and hydrogen into the fine chemicals hydroxyectoine and ectoine. Bioresour Technol 374:128753. https://doi.org/10.1016/j.biortech.2023.128753
Cappelletti M, Zampolli J, Di Gennaro P, Zannoni D (2019) Genomics of Rhodococcus. Biology of Rhodococcus, 2nd edn. Springer International Publishing, pp 23–60. https://doi.org/10.1007/978-3-030-11461-9_2
Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368. https://doi.org/10.1007/BF00129093
Chen T, Zhang H, Liu Y, Liu YX, Huang L (2021) EVenn: Easy to create repeatable and editable Venn diagrams and Venn networks online. J Genet Genomics 48:863–866. https://doi.org/10.1016/j.jgg.2021.07.007
Cho MA, Han S, Lim YR, Kim V, Kim H, Kim D (2019) Streptomyces cytochrome P450 enzymes and their roles in the biosynthesis of macrolide therapeutic agents. Biomol Ther (Seoul) 27:127–133. https://doi.org/10.4062/biomolther.2018.183
R Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. https://www.R-project.org
Das N, Basak LVG, Salam JA, Abigail EA (2012) Application of biofilms on remediation of pollutants - an overview. J Microbiol Biotechnol 2:783–790
Dash HR, Mangwani N, Chakraborty J, Kumari S, Das S (2013) Marine bacteria: potential candidates for enhanced bioremediation. Appl Microbiol Biotechnol 97:561–571. https://doi.org/10.1007/s00253-012-4584-0
de Carvalho CCCR (2012) Adaptation of Rhodococcus erythropolis cells for growth and bioremediation under extreme conditions. Res Microbiol 163:125–136. https://doi.org/10.1016/j.resmic.2011.11.003
de Carvalho CCCR, Costa SS, Fernandes P, Couto I, Viveiros M (2014) Membrane transport systems and the biodegradation potential and pathogenicity of genus Rhodococcus. Front Physiol 5:133. https://doi.org/10.3389/fphys.2014.00133
De Coster W (2018) Nanoplot: Plotting tool for long read sequencing data and alignments. Available on GitHub: https://github.com/wdecoster/NanoPlot
DeBruyn JF, Mead TM, Sayler GS (2011) Horizontal transfer of PAH catabolism genes in Mycobacterium: evidence from Comparative Genomics and isolated pyrene-degrading Bacteria. Environ Sci Technol 46:99–106. https://doi.org/10.1021/es201607y
Denaro R, Crisafi F, Russo D, Genovese M, Messina E, Genovese L, Carbone M, Ciavatta ML, Ferrer M, Golyshin P, Yakimov MM (2014) Alcanivorax borkumensis produces an extracellular siderophore in iron-limitation condition maintaining the hydrocarbon-degradation efficiency. Mar Genomics 17:43–52. https://doi.org/10.1016/j.margen.2014.07.004
Dhaouadi S, Mougou AH, Wu CJ, Gleason ML, Rhouma A (2020) Sequence analysis of 16S rDNA, gyrB and alkB genes of plant-associated Rhodococcus species from Tunisia. Int J Syst Evol Microbiol 70:6491–6507. https://doi.org/10.1099/ijsem.0.004521
Dodd A, Swanevelder D, Zhou N, Brady D, Hallsworth JE, Rumbold K (2018) Streptomyces albulus yields ε-poly-L-lysine and other products from salt-contaminated glycerol waste. J Ind Microbiol Biotechnol 45:1083–1090. https://doi.org/10.1007/s10295-018-2082-9
Emms DM, Kelly S (2018) STAG: species tree inference from all genes. bioRxiv. https://www.biorxiv.org/content/10.1101/267914v1
Emms DM, Kelly S (2019) OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 20:238. https://doi.org/10.1186/s13059-019-1832-y
Fahy A, Ball AS, Lethbridge G, Timmis KN, McGenity TJ (2008) Isolation of alkali-tolerant benzene-degrading bacteria from a contaminated aquifer. Lett Appl Microbiol 47:60–66. https://doi.org/10.1111/j.1472-765X.2008.02386.x
Francis IM, Vereecke B (2019) Plant-associated Rhodococcus species, for better and for worse. Biology of Rhodococcus, 2nd edn. Springer International Publishing, pp 359–377. https://doi.org/10.1007/978-3-030-11461-9_13
Fuentes S, Barra B, Caporaso JG, Seeger M (2016) From rare to dominant: a fine-tuned soil bacterial bloom during petroleum hydrocarbon bioremediation. Appl Environ Microbiol 82:888–896. https://doi.org/10.1128/AEM.02625-15
Gordillo F, Chávez FP, Jerez CA (2007) Motility and chemotaxis of Pseudomonas sp. B4 towards polychlorobiphenyls and chlorobenzoates. FEMS Microbiol Ecol 60:322–328. https://doi.org/10.1111/j.1574-6941.2007.00293.x
Goudriaan M, Morales VH, van der Meer MTJ, Mets A, Ndhlovu RT, van Heerwaarden J, Simon S, Heuer VB, Hinrichs KU, Niemann H (2023) A stable isotope assay with 13C-labeled polyethylene to investigate plastic mineralization mediated by Rhodococcus ruber. Mar Pollut Bull 186:114369. https://doi.org/10.1016/j.marpolbul.2022.114369
Guevara G, Castillo Lopez M, Alonso S, Perera J, Navarro-Llorens JM (2019) New insights into the genome of Rhodococcus ruber strain Chol-4. BMC Genomics 20:332. https://doi.org/10.1186/s12864-019-5677-2
Gupta VK, Chaudhari NM, Iskepalli S, Dutta C (2015) Divergences in gene repertoire among the reference Prevotella genomes derived from distinct body sites of human. BMC Genomics 16:153. https://doi.org/10.1186/s12864-015-1350-6
Hara H, Stewart GR, Mohn WW (2010) Involvement of a novel ABC transporter and monoalkyl phthalate ester hydrolase in phthalate ester catabolism by Rhodococcus jostii RHA1. Appl Environ Microbiol 76:1516–1523. https://doi.org/10.1128/AEM.02621-09
Hassanshahian M, Zeynalipour MS, Musa FH (2014) Isolation and characterization of crude oil degrading bacteria from the Persian Gulf (Khorramshahr provenance). Mar Pollut Bull 82:39–44. https://doi.org/10.1016/j.marpolbul.2014.03.027
Kafilzadeh F (2015) Distribution and sources of polycyclic aromatic hydrocarbons in water and sediments of the Soltan Abad River, Iran. Egypt J Aquat Res 41:227–231. https://doi.org/10.1016/j.ejar.2015.06.004
Kim DW, Lee K, Lee DH, Cha CJ (2018) Comparative genomic analysis of pyrene-degrading Mycobacterium species: genomic islands and ring-hydroxylating dioxygenases involved in pyrene degradation. J Microbiol 56:798–804. https://doi.org/10.1007/s12275-018-8372-0
Kitamura Y, Sawabe E, Ohkusu K, Tojo N, Tohda S (2012) First report of sepsis caused by Rhodococcus corynebacterioides in a patient with myelodysplastic syndrome. J Clin Microbiol 50:1089–1091. https://doi.org/10.1128/JCM.06279-11
Krell T, Lacal J, Reyes-Darias JA, Jimenez-Sanchez C, Sungthong R, Ortega-Calvo JJ (2013) Bioavailability of pollutants and chemotaxis. Curr Opin Biotechnol 24:451–456. https://doi.org/10.1016/j.copbio.2012.08.011
Kumari A, Upadhyay V, Kumar S (2023) A critical insight into occurrence and fate of polycyclic aromatic hydrocarbons and their green remediation approaches. Chemosphere 329:138579. https://doi.org/10.1016/j.chemosphere.2023.138579
Kuyukina MS, Ivshina IB (2010) Rhodococcus biosurfactants: biosynthesis, properties, and potential applications. In: Alvarez HM (ed) Biology of Rhodococcus, 1st edn. Springer-, Berlin, pp 291–313. https://doi.org/10.1007/978-3-642-12937-7_11
Kwasiborski A, Mondy S, Chong TM, Chan KG, Beury-Cirou A, Faure D (2015) Core genome and plasmidome of the quorum-quenching bacterium Rhodococcus erythropolis. Genetica 143:253–261. https://doi.org/10.1007/s10709-015-9827-4
Ladino-Orjuela G, Gomes E, da Silva R, Salt C, Parsons JR (2016) Metabolic pathways for degradation of aromatic hydrocarbons by bacteria. Rev Environ Contam Toxicol 237:105–121. https://doi.org/10.1007/978-3-319-23573-8_5
Larkin MJ, Kulakov LA, Allen CCR (2005) Biodegradation and Rhodococcus - Masters of catabolic versatility. Curr Opin Biotechnol 16:282–290. https://doi.org/10.1016/j.copbio.2005.04.007
Ławniczak Ł, Woźniak-Karczewska M, Loibner AP, Heipieper HJ, Chrzanowski Ł (2020) Microbial Degradation of hydrocarbons-Basic principles for Bioremediation: a review. Molecules 25:856. https://doi.org/10.3390/molecules25040856
Lechner M, Findeiss S, Steiner L, Marz M, Stadler PF, Prohaska SJ (2011) Proteinortho: detection of (co-)orthologs in large-scale analysis. BMC Bioinformatics 12:124. https://doi.org/10.1186/1471-2105-12-124
Lefort V, Desper R, Gascuel O (2015) FastME 2.0: a comprehensive, accurate, and fast distance-bases phylogeny inference program. Mo Bio Evol 32:2798–2800. https://doi.org/10.1093/molbev/msv150
Liu J, Zhang A-N, Yong-Jun L, Zhe L, Yu L, Wu Xi-Jun (2021) Analysis of the mechanism for enhanced pyrene biodegradation base on interactions between iron-ions and Rhodococcus ruber strain L9. Ecotoxicol Environ Saf 225:112789. https://doi.org/10.1016/j.ecoenv.2021.112789
Luo A, Wu YR, Xu Y, Kan J, Qiao J, Liang L, Huang T, Hu Z (2016) Characterization of a cytochrome P450 monooxygenase capable of high molecular weight PAHs oxidization from Rhodococcus sp. P14. Process Biochem 51:2127–2133. https://doi.org/10.1016/j.procbio.2016.07.024
Martínková L, Uhnáková B, Pátek M, Nešvera J, Křen V (2009) Biodegradation potential of the genus Rhodococcus. Environ Int 35:162–177. https://doi.org/10.1016/j.envint.2008.07.018
McGenity TJ, Whitby C, Fahy A (2010) Alkaliphilic hydrocarbon degraders. In: Timmis KN (ed) Handbook of hydrocarbon and lipid Microbiology. Springer, Berlin, Heidelberg, pp 1931–1937. https://doi.org/10.1007/978-3-540-77587-4_141
Mcleod MP, Warren RL, Hsiao WWL, Araki N, Myhre M, Fernandes C, Miyazawa D, Wong W, Lillquist AL, Wang D, Dosanjh M, Hara H, Petrescu A, Morin RD, Yang G, Stott JM, Schein JE, Shin H, Smailus D, Siddiqui AS, Marra MA, Jones SJM, Holt R, Brinkman FSL, Miyauchi K, Fukuda M, Davies JE, Mohn WW, Eltis LD (2006) The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci USA 103:15582–15587. https://doi.org/10.1073/pnas.0607048103
Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 10:2182. https://doi.org/10.1038/s41467-019-10210-3
Meng Q, Ren H, Lv F, Li S, Huang H, Liu Z, Cao F, Zhu T, Yin J, Chen B, Yu J, Yu Z (2024) Major facilitator superfamily transporter PhaT modulates the efflux and degradation of polycyclic aromatic hydrocarbons in Novosphingobium pentaromativorans US6-1. Process Biochem 142:194–203. https://doi.org/10.1016/j.procbio.2024.04.023
Mohapatra B, Phale PS (2021) Microbial degradation of naphthalene and substituted naphthalenes: metabolic diversity and genomic insight for bioremediation. Front Bioeng Biotechnol 9:602445. https://doi.org/10.3389/fbioe.2021.602445
Nazari MT, Simon V, Machado BS, Crestani L, Marchezi G, Concolato G, Ferrari V, Colla LM, Piccin JS (2022) Rhodococcus: a promising genus of actinomycetes for the bioremediation of organic and inorganic contaminants. J Environ Manag 323:116220. https://doi.org/10.1016/j.jenvman.2022.116220
Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, O’Hara R, Solymos P, Stevens M, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, De Caceres M, Durand S, Evangelista H, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill M, Lahti L, McGlinn D, Ouellette M, Ribeiro-Cunha E, Smith T, Stier A, Ter Braak C, Weedon J (2022) vegan: Community Ecology Package. R package version 2.6-4. https://cran.r-project.org/web/packages/vegan/index.html
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055. https://doi.org/10.1101/gr.186072.114
Peng T, Kan J, Hu J, Hu Z (2020) Genes and novel sRNAs involved in PAHs degradation in marine bacteria Rhodococcus sp. P14 revealed by the genome and transcriptome analysis. 3 Biotech 10:140. https://doi.org/10.1007/s13205-020-2133-6
Philp JC, Kuyukina MS, Ivshina IB, Dunbar SA, Christofi N, Lang S, Wray V (2002) Alkanotrophic Rhodococcus ruber as a biosurfactant producer. Appl Microbiol Biotechnol 59:318–324. https://doi.org/10.1007/s00253-002-1018-4
Prešern U, Goličnik M (2023) Enzyme databases in the era of omics and artificial intelligence. Int J Mol Sci 24:16918. https://doi.org/10.3390/ijms242316918
Rai D, Mehra S (2021) The mycobacterial efflux pump EfpA can induce high drug tolerance to many antituberculosis drugs, including moxifloxacin, in Mycobacterium smegmatis. Antimicrob Agents Chemother 65:e0026221. https://doi.org/10.1128/AAC.00262-21
Ravindra K, Sokhi R, Grieken RV (2008) Atmospheric polycyclic aromatic hydrocarbons: source attribution, emission factors and regulation. Atmos Environ 42:2895–2921. https://doi.org/10.1016/j.atmosenv.2007.12.010
Rojas-Vargas J, Adaya L, Silva-Jiménez H, Licea-Navarro AF, Sanchez-Flores A, Gracia A, Pardo-López L (2022) Oil-degrading bacterial consortium from Gulf of Mexico designed by a factorial method, reveals stable population dynamics. Front Mar Sci 9:962071. https://doi.org/10.3389/fmars.2022.962071
Rojas-Vargas J, Castelán-Sánchez HG, Pardo-López L (2023) HADEG: a curated hydrocarbon aerobic degradation enzymes and genes database. Comput Biol Chem 107:107966. https://doi.org/10.1016/j.compbiolchem.2023.107966
Sakshi, Singh SK, Haritash AK (2022) Evolutionary relationship of polycyclic aromatic hydrocarbons degrading bacteria with strains isolated from petroleum contaminated soil based on 16S rRNA diversity. Polycycl Aromat Compd 42:2045–2058. https://doi.org/10.1080/10406638.2020.1825003
Samanta SK, Singh OV, Jain RK (2002) Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Microbiol 20:243–248. https://doi.org/10.1016/S0167-7799(02)01943-1
Satpute SK, Bhawsar PK, Dhakephalkar PK, Chopade BA (2008) Assessment of different screening methods for selecting biosurfactant producing marine bacteria. Indian J Mar Sci 37:243–250
Seemann T (2014) Prokka: Rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. https://doi.org/10.1093/bioinformatics/btu153
Segura A, Molina L, Ramos JL (2014) Plasmid-mediated tolerance toward environmental pollutants. Microbiol Spectr 2. https://doi.org/10.1128/microbiolspec.plas-0013-2013
Silva-Jiménez H, Araujo-Palomares CL, Macías-Zamora JV, Ramírez-Álvarez N, García-Lara B, Corrales-Escobosa AR (2018) Identification by MALDI-TOF MS of environmental bacteria with high potential to degrade pyrene. J Mex Chem Soc 62. https://doi.org/10.29356/jmcs.v62i2.411
Soldatou S, Eldjárn GH, Ramsay A, van der Hooft JJJ, Hughes AH, Rogers S, Duncan KR (2021) Comparative metabologenomics analysis of polar actinomycetes. Mar Drugs 19:103. https://doi.org/10.3390/md19020103
Sun R, Sun Y, Li QX, Zheng X, Luo X, Mai B (2018) Polycyclic aromatic hydrocarbons in sediments and marine organisms: implications of anthropogenic effects on the coastal environment. Sci Total Environ 640–641:264–272. https://doi.org/10.1016/j.scitotenv.2018.05.320
Táncsics A, Benedek T, Szoboszlay S, Veres PG, Farkas M, Máthé I, Márialigeti K, Kukolya J, Lányi S, Kriszt B (2015) The detection and phylogenetic analysis of the alkane 1-monooxygenase gene of members of the genus Rhodococcus. Syst Appl Microbiol 38:1–7. https://doi.org/10.1016/j.syapm.2014.10.010
Undabarrena A, Salvà-Serra F, Jaén-Luchoro D, Castro-Nallar E, Mendez KN, Valencia R, Ugalde JA, Moore ERB, Seeger M, Cámara B (2018) Complete genome sequence of the marine Rhodococcus sp. H-CA8f isolated from Comau fjord in Northern Patagonia, Chile. Mar Genomics 40:13–17. https://doi.org/10.1016/j.margen.2018.01.004
Undabarrena A, Valencia R, Cumsille A, Zamora-Leiva L, Castro-Nallar E, Barona-Gomez F, Cámara B (2021) Rhodococcus comparative genomics reveals a phylogenomic-dependent non-ribosomal peptide synthetase distribution: insights into biosynthetic gene cluster connection to an orphan metabolite. Microb Genom 7:000621. https://doi.org/10.1099/mgen.0.000621
US EPA 8015B (1996) Nonhalogenated organics using GC/FID. EEUU. https://archive.epa.gov/epawaste/hazard/testmethods/web/pdf/method%208015b,%20revision%202%20-%201996.pdf. (accessed 22 June of 2023)
Van Arnam EB, Ruzzini AC, Sit CS, Horn H, Pinto-Tomás AA, Currie CR, Clardy J (2016) Selvamicin, an atypical antifungal polyene from two alternative genomic contexts. Proc Natl Acad Sci USA 113:12940–12945. https://doi.org/10.1073/pnas.1613285113
Vernikos GS (2020) A review of pangenome tools and recent studies. In: Tettelin H, Medini D, editors. The Pangenome: Diversity, Dynamics and Evolution of Genomes Springer, pp 89–112. https://doi.org/10.1007/978-3-030-38281-0
Vila J, Tauler M, Grifoll M (2015) Bacterial PAH degradation in marine and terrestrial habitats. Curr Opin Biotechnol 33:95–102. https://doi.org/10.1016/j.copbio.2015.01.006
Walter U, Beyer M, Klein J, Rehm HJ (1991) Degradation of pyrene by Rhodococcus sp. UW1. Appl Microbiol Biotechnol 34:671–676 017575989100048Z
Ward AL, Reddyvari P, Borisova R, Shilabin AG, Lampson BC (2018) An inhibitory compound produced by a soil isolate of Rhodococcus has strong activity against the veterinary pathogen R. Equi. PLoS ONE 13:e0209275. https://doi.org/10.1371/journal.pone.0209275
Wick RR, Judd LM, Gorrie CL, Holt KE (2017) Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 13:e1005595. https://doi.org/10.1371/journal.pcbi.1005595
Xiao Y, Jiang R, Wu X, Zhong Q, Li Y, Wang H (2021) Comparative genomic analysis of Stenotrophomonas maltophilia strain W18 reveals its adaptative genomic features for degrading polycyclic aromatic hydrocarbons. Microbiol Spectr 9:e01420–e01421. https://doi.org/10.1128/Spectrum.01420-21
Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil-degrading marine bacteria. Curr Opin Biotechnol 18:257–266. https://doi.org/10.1016/j.copbio.2007.04.006
Yang HY, Jia RB, Chen B, Li L (2014) Degradation of recalcitrant aliphatic and aromatic hydrocarbons by a dioxin-degrader Rhodococcus sp. strain p52. Environ Sci Pollut Res 21:11086–11093. https://doi.org/10.1007/s11356-014-3027-0
Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286. https://doi.org/10.1007/s10482-017-0844-4
Zada S, Zhou H, Xie J, Hu Z, Ali S, Sajjad W, Wang H (2021) Bacterial degradation of pyrene: biochemical reactions and mechanisms. Int Biodeterior Biodegrad 162:105233. https://doi.org/10.1016/j.ibiod.2021.105233
Zampolli J, Zeaiter Z, Di Canito A, Di Gennaro P (2019) Genome analysis and -omics approaches provide new insights into the biodegradation potential of Rhodococcus. Appl Microbiol Biotechnol 103:1069–1080. https://doi.org/10.1007/s00253-018-9539-7
Zampolli J, Orro A, Vezzini D, Di Gennaro P (2023) Genome-based exploration of Rhodococcus species for plastic-degrading genetic determinants using bioinformatic analysis. Microorganisms 10:1846. https://doi.org/10.3390/microorganisms10091846
Zeng EY, Vista CL (1997) Organic pollutants in the coastal environment off San Diego, California. 1. Source identification and assessment by compositional indices of polycyclic aromatic hydrocarbons. Environ Toxicol Chem 16:179–188. https://doi.org/10.1002/etc.5620160212
Zhang Y, Qin F, Qiao J, Li G, Shen C, Huang T, Hu Z (2012) Draft genome sequence of Rhodococcus sp. Strain P14, a biodegrader of high-molecular-weight polycyclic aromatic hydrocarbons. J Bacteriol 194:3546. https://doi.org/10.1128/JB.00555-12
Zhang L, Yang L, Zhou Q, Zhang X, Xing W, Wei Y, Hu M, Zhao L, Toriba A, Hayakawa K, Tang N (2020) Size distribution of particulate polycyclic aromatic hydrocarbons in fresh combustion smoke and ambient air: a review. J Environ Sci (China) 88:370–384. https://doi.org/10.1016/j.jes.2019.09.007
Zhao Y, Jia X, Yang J, Ling Y, Zhang Z, Yu J, Wu J, Xiao J (2014) PanGP: a tool for quickly analyzing bacterial pan-genome profile. Bioinformatics 30:1297–1299. https://doi.org/10.1093/bioinformatics/btu017
Zhao T, Gao Y, Yu T, Zhang Y, Zhang Z, Zhang L, Zhang L (2021) Biodegradation of phenol by a highly tolerant strain Rhodococcus ruber C1: biochemical characterization and comparative genome analysis. Ecotoxicol Environ Saf 208:111709. https://doi.org/10.1016/j.ecoenv.2020.111709
Acknowledgements
The authors thank the Unidad de Secuenciación Masiva y Bioinformática-IBt-UNAM, especially Karel Estrada and Jerome Verleyen, for their bioinformatic and high-performance support, respectively. RAB-G appreciates the Sabbatical fellowship (CVU 389616) granted by CONACyT (currently CONAHCyT) and to the RYC2022-037554-I project funded by MCIN/AEI/10.13039/501100011033 and FSE+. SE-J, TM-P, and GC-H received postdoctoral fellowships from CONACyT (CONAHCyT).
Funding
This research was funded by the Program for the Professional Development of Teachers for Higher Education (PRODEP) of the Mexican Ministry of Public Education (project UABC-PTC-621) and Universidad Autónoma de Baja California (project IIO-UABC 403/1751).
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SE-J: Investigation, Data curation, Formal analysis, Visualization, Writing – original draft preparation, Writing – review & editing. CLA-P: Investigation, Visualization, Writing – original draft preparation. TM-P: Data curation, Formal analysis, Visualization, Writing – review & editing. NR-A: Formal analysis, Validation, Writing – review & editing. CQ-H: Investigation. RAB-G: Data curation, Writing – review & editing. AS-F: Data curation, Resources, Writing – review & editing. GC-H: Writing – review & editing. HS-J: Conceptualization, Formal analysis, Funding acquisition, Project administration, Resources, Validation, Visualization, Writing – original draft preparation, Writing – review & editing. All authors reviewed the manuscript.
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Embarcadero-Jiménez, S., Araujo-Palomares, C.L., Moreno-Perlín, T. et al. Physiology and comparative genomics of the haloalkalitolerant and hydrocarbonoclastic marine strain Rhodococcus ruber MSA14. Arch Microbiol 206, 328 (2024). https://doi.org/10.1007/s00203-024-04050-z
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DOI: https://doi.org/10.1007/s00203-024-04050-z