Genome-Resolved Meta-Analysis of the Microbiome in Oil Reservoirs Worldwide

Abstract

Microorganisms inhabiting subsurface petroleum reservoirs are key players in biochemical transformations. The interactions of microbial communities in these environments are highly complex and still poorly understood. This work aimed to assess publicly available metagenomes from oil reservoirs and implement a robust pipeline of genome-resolved metagenomics to decipher metabolic and taxonomic profiles of petroleum reservoirs worldwide. Analysis of 301.2 Gb of metagenomic information derived from heavily flooded petroleum reservoirs in China and Alaska to non-flooded petroleum reservoirs in Brazil enabled us to reconstruct 148 metagenome-assembled genomes (MAGs) of high and medium quality. At the phylum level, 74% of MAGs belonged to bacteria and 26% to archaea. The profiles of these MAGs were related to the physicochemical parameters and recovery management applied. The analysis of the potential functional core in the reservoirs showed that the microbiota was specialized for each site, with 31.7% of the total KEGG orthologies annotated as functions (1690 genes) common to all oil fields, while 18% of the functions were site-specific, i.e., present only in one of the oil fields. The oil reservoirs with a lower level of intervention were the most similar to the potential functional core, while the oil fields with a long history of water injection had greater variation in functional profile. These results show how key microorganisms and their functions respond to the distinct physicochemical parameters and interventions of the oil field operations such as water injection and expand the knowledge of biogeochemical transformations in these ecosystems.

Environmental Selection and Biogeography Shape the Microbiome of Subsurface Petroleum Reservoirs

“…4 ). These results are consistent with observations of high proportions of genes for enzymes involved in aerobic hydrocarbon metabolism in various anaerobic hydrocarbon resource environments including oil reservoirs ( 29 , 49 ) and may arise from the enrichment of initially minor groups of organisms capable of aerobic respiration coming into contact with air during sampling and sample transport. This is substantiated by genes encoding alkane hydroxylase ( alkB ) and monoaromatic dioxygenase (MAH) showing high-sequence identity (based on BLAST against the nonredundant nucleotide database) with Marinobacter spp., which are generally detected in low relative abundance in situ by 16S rRNA gene amplicon sequencing ( Table S5 ).…”

“…The hydrocarbon activation genes assA , bssA , and nmsA were only detected in one-quarter of the oil reservoirs examined by metagenome sequencing in this study. A similar result was reported by Hidalgo et al ( 29 ) who found only two bssA genes in 148 MAGs from different oil reservoirs using KEGG assignments. The discrepancy of widespread genomic potential for methanogenesis and geochemical evidence of biogenic methane production in reservoirs ( 37 , 38 ) on the one hand, and limited occurrences of anaerobic hydrocarbon degradation genes on the other, hints that other mechanisms for anaerobic hydrocarbon biodegradation ( 39 – 41 ) or as-yet undetected hydrocarbon activation genes in anoxic petroleum reservoirs.…”

“…Some inconsistency between these two metagenome analysis strategies may be expected to arise based on preferential assembly of the most abundant organisms in genome-centric analyses resulting in an associated loss of unbinned sequence information in the process. For example, MAGs containing genes for dissimilatory sulfate reduction were identified in just over half of the oil fields in the genome-centric study ( 29 ) whereas in the analysis performed here, by avoiding genome binning, sulfate reduction genes were identified in 24 out of 25 samples. Similarly, genome-centric analysis suggested that sulfide oxidation was not widespread in oil fields ( 29 ), whereas the less restrictive analysis of unassembled contigs in the present study suggests a universal genetic potential for sulfide oxidation in oil reservoirs.…”

“…Diverse genes encode functions for processes such as fermentation, sulfate reduction, hydrocarbon biodegradation, and methanogenesis in the oil reservoir microbiome. These and other metabolic functions were highlighted in a similar meta-analysis of oil reservoir metagenome-assembled genomes (MAGs) by Hidalgo et al ( 29 ) that focused on nine different oil reservoirs in China, Alaska’s North Slope, and offshore Brazil. That genome-centric approach revealed both core and environment-specific functions but also included observations that differ from those in the gene-centric analysis presented here with respect to the metabolisms noted above.…”

Disentangling the microbial genomic traits associated with aromatic hydrocarbon degradation in a jet fuel-contaminated aquifer

“…This phylum is characterized by small cell and genome sizes(Tian et al 2020;Hidalgo et al 2021), carrying only essential genes and lacking a lot of metabolic functions(Hidalgo et al 2021;Brown et al 2015). For this reason, some authors have proposed that members of this phylum have a symbiont lifestyle(Castelle et al 2018;Hidalgo et al 2021).…”