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Physiology and comparative genomics of the haloalkalitolerant and hydrocarbonoclastic marine strain Rhodococcus ruber MSA14

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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

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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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Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Hortencia Silva-Jiménez.

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The authors declare no competing interests.

Additional information

Communicated by Dmitriy Volokhov.

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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

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