Genome-resolved analyses show an extensive diversification in key aerobic hydrocarbon-degrading enzymes across bacteria and archaea

Background Hydrocarbons (HCs) are organic compounds composed solely of carbon and hydrogen that are mainly accumulated in oil reservoirs. As the introduction of all classes of hydrocarbons including crude oil and oil products into the environment has increased significantly, oil pollution has become a global ecological problem. However, our perception of pathways for biotic degradation of major HCs and key enzymes in these bioconversion processes has mainly been based on cultured microbes and is biased by uneven taxonomic representation. Here we used Annotree to provide a gene-centric view of the aerobic degradation ability of aliphatic and aromatic HCs in 23,446 genomes from 123 bacterial and 14 archaeal phyla. Results Apart from the widespread genetic potential for HC degradation in Proteobacteria, Actinobacteriota, Bacteroidota, and Firmicutes, genomes from an additional 18 bacterial and 3 archaeal phyla also hosted key HC degrading enzymes. Among these, such degradation potential has not been previously reported for representatives in the phyla UBA8248, Tectomicrobia, SAR324, and Eremiobacterota. Genomes containing whole pathways for complete degradation of HCs were only detected in Proteobacteria and Actinobacteriota. Except for several members of Crenarchaeota, Halobacterota, and Nanoarchaeota that have tmoA, ladA, and alkB/M key genes, respectively, representatives of archaeal genomes made a small contribution to HC degradation. None of the screened archaeal genomes coded for complete HC degradation pathways studied here; however, they contribute significantly to peripheral routes of HC degradation with bacteria. Conclusion Phylogeny reconstruction showed that the reservoir of key aerobic hydrocarbon-degrading enzymes in Bacteria and Archaea undergoes extensive diversification via gene duplication and horizontal gene transfer. This diversification could potentially enable microbes to rapidly adapt to novel and manufactured HCs that reach the environment

Distinct microbial community along the chronic oil pollution continuum of the Persian Gulf converge with oil spill accidents

The Persian Gulf, hosting ca. 48% of the world's oil reserves, has been chronically exposed to natural oil seepage. Oil spill studies show a shift in microbial community composition in response to oil pollution; however, the influence of chronic oil exposure on the microbial community remains unknown. We performed genome-resolved comparative analyses of the water and sediment samples along Persian Gulf's pollution continuum (Strait of Hormuz, Asalouyeh, and Khark Island). Continuous exposure to trace amounts of pollution primed the intrinsic and rare marine oil-degrading microbes such as Oceanospirillales, Flavobacteriales, Alteromonadales, and Rhodobacterales to bloom in response to oil pollution in Asalouyeh and Khark samples. Comparative analysis of the Persian Gulf samples with 106 oil-polluted marine samples reveals that the hydrocarbon type, exposure time, and sediment depth are the main determinants of microbial response to pollution. High aliphatic content of the pollution enriched for Oceanospirillales, Alteromonadales, and Pseudomonadales whereas, Alteromonadales, Cellvibrionales, Flavobacteriales, and Rhodobacterales dominate polyaromatic polluted samples. In chronic exposure and oil spill events, the community composition converges towards higher dominance of oil-degrading constituents while promoting the division of labor for successful bioremediation

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Additional file 1 of Genome-resolved analyses show an extensive diversification in key aerobic hydrocarbon-degrading enzymes across bacteria and archaea

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Additional file 9 of Genome-resolved analyses show an extensive diversification in key aerobic hydrocarbon-degrading enzymes across bacteria and archaea

Additional file 9: Supplementary Figure S1. Schematic representation of HC degradation pathways studied in this work. Purple circles show key HC degrading enzymes trigerring the degradation. Blue circles are other crucial enzymes. Important intermediate compounds are written in blue. Supplementary Figure S2. Distribution of 143512 genomes of the GTDB database release 89 in different phyla. Supplementary Figure S3. Distribution of aliphatic hydrocarbon-degrading genes across domain bacteria at the phylum level. In plot A, the color gradient indicates the proportion of degrading members of each phylum to the entire HC degrading community. In plot B, the color gradient shows the percentage of HC degrading members of each phylum. Columns are the name of genes involved in HC degradation, which key ones are represented in red. Supplementary Figure S4. Distribution of aromatic hydrocarbon-degrading genes across domain bacteria at the phylum level. In plot A, the color gradient indicates the proportion of degrading members of each phylum to the entire HC degrading community. In plot B, the color gradient shows the percentage of HC degrading members of each phylum. Columns are the name of genes involved in HC degradation, which key ones are represented in red. Enzymes written in blue are shared among the degradation processes of different aromatic compounds (xylene, phenol and naphthalene). Supplementary Figure S5. Distribution of aliphatic hydrocarbon-degrading genes across domain archaea at the phylum level. In plot A, the color gradient indicates the proportion of degrading members of each phylum to the entire HC degrading community. In plot B, the color gradient shows the percentage of HC degrading members of each phylum. Columns are the name of genes involved in HC degradation, which key ones are represented in red. Supplementary Figure S6. Distribution of aromatic hydrocarbon-degrading genes across domain archaea at the phylum level. In plot A, the color gradient indicates the proportion of degrading members of each phylum to the entire HC degrading community. In plot B, the color gradient shows the percentage of HC degrading members of each phylum. Columns are the name of genes involved in HC degradation, which key ones are represented in red. Enzymes with blue color are shared among the degradation processes of different aromatic compounds (xylene, phenol and naphthalene). Supplementary Figure S7. Network interaction between 18 copies of xylX gene in Immundisolibacter cernigliae and other genomes with more than two copies of this gene. Only the blast identity values between 50 to 100 percent are shown. Edges are color-coded based on their blast identity. The size of nodes is based on the “Degree,” which is determined by the number of edges of each node. Edges in red are versions of xylX in Immundisolibacter cernigliae that had a higher degree than others. The gene ID of the assigned number of each node is represented in Supplementary Table S7. Supplementary Figure S8. Distribution of genome size versus GC content of the studied genomes with key HC degrading genes. Supplementary Figure S9. Distribution of aliphatic (A) and aromatic (B) hydrocarbon-degrading genes across domain archaea at the phylum level. Columns show the name of genes involved in HC degradation and are represented in different colors for various compounds. The color gradient for genes of each compound indicates the percentage of HC degrading members of each phylum. Supplementary Figure S10. The overview of workflow that has been done in the present study

Additional file 2 of Genome-resolved analyses show an extensive diversification in key aerobic hydrocarbon-degrading enzymes across bacteria and archaea

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