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

Abstract

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.

The trade-off between individual metabolic specialization and versatility determines the metabolic efficiency of microbial communities

“…In contrast, most microbes lack a complete set of enzymes. Instead, many microbes contain a subset for hydrocarbon degradation, an observation that is in agreement with findings in several previous studies [21][22][23][24] , suggesting that MDOL is prevalent in hydrocarbon degradation. When we assessed three degrading pathways of aromatic hydrocarbons, we found that most microbes only perform one single metabolic step (toluene: 80.3 %, Figure 7E; biphenyl: 86.6 %, Figure 7G; naphthalene: 72.9 %, Figure 7H).…”

“…We divided these pathways into several steps according to the following two conditions: (1) whether the selected intermediates are chemically stable and (2) whether the intermediates can be transported across the cell membrane so that be exchanged among different populations (Figure S13). To identify the distribution of the genes encoding the enzymes responsible for every metabolic step in microbial genomes, we searched for the hydrocarbon degradation genes in a database recently built from 24,692 publicly available archaeal (n = 1246) and bacterial (n = 23,446) genomes 21 . Based on these analyses, we classified these microorganisms into different genotypes that can perform one or multiple metabolic steps, which are conceptualized by bit strings containing "0", "1", "A" and "B" (Figure 7; Methods).…”

“…The analysis was performed based on a database compiled recently 21 , which used Annotree to annotate the genes encoding the aerobic degradation pathways of aliphatic (short-chain and long-chain n-alkanes, as well as cycloalkane) and aromatic (toluene, phenol, xylene, benzene, biphenyl, and naphthalene) hydrocarbons in 24,692 genomes from 123 bacterial and 14 archaeal phyla. The database was further analyzed in this work.…”

Genome-Centric Metatranscriptomics Reveals Multiple Co-occurring Routes for Hydrocarbon Degradation in Chronically Contaminated Marine Microbial Mats

“…In addition, AAI and ANI comparisons revealed that Pseudomonadales and Halieaceae populations that were only detected in EDB or SL mats were affiliated with different putative genera depending on the mats. These lineages, frequently identified as hydrocarbon degraders in contaminated aerobic systems, were found to degrade a large variety of petroleum compounds in marine biomes. ,, Therefore, this contrast between EDB and SL populations, which was not detectable by 16S rRNA and functional gene sequencing, suggests a fine selection of the Pseudomonadales and Halieaceae populations by the hydrocarbon content, leading to the growth of populations with similar gene content ( alkB and/or CYP153) but distinct substrate affinity. Together our results suggest that the detection of hydrocarbon degradation genes could not differentiate chronic to punctual hydrocarbon contamination and that an in-depth analysis of the microbiome combined with transcriptomic data are required to identify indicators of long-term hydrocarbon pollution in microbial mat ecosystems.…”

Crude Oil Degradation in Temperatures Below the Freezing Point by Bacteria from Hydrocarbon-Contaminated Arctic Soils and the Genome Analysis of Sphingomonas sp. AR_OL41

“…Bacteria of the genera Pseudomonas and Sphingomonas were also detected during metagenomic analysis of samples of ground soils and seawater, sea ice, and crude oil encapsulating the sea ice of the Arctic region [ 28 , 29 ]. The use of n -alkanes and other petroleum components has been shown for members of the genera Pseudomonas , Rhodococcus , and Arthrobacter [ 30 , 31 , 32 , 33 , 34 ], whereas for bacteria of the genus Sphingomonas , this property is rare [ 35 , 36 , 37 , 38 ]. In order to determine how well the isolated four strains are adapted to the habitat conditions, the growth of the strains in oil at low temperatures (9 and −1.5 °C) was studied, and physiological and metabolic properties (temperature and salinity ranges for growth, the spectrum of enzymes, the substrates used, differences from type strains of respective species) were determined.…”