Metagenomic characterization reveals complex association of soil hydrocarbon-degrading bacteria

Ruiz, Oscar N.; Brown, Lisa M.; Radwan, Osman; Bowen, Loryn L.; Gunasekera, Thusitha S.; Mueller, Susan S.; West, Zachary J.; Striebich, Richard C.

doi:10.1016/j.ibiod.2020.105161

Cited by 22 publications

(5 citation statements)

References 51 publications

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“…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).…”

Section: Species Exhibiting Metabolic Versatility While Being Non-aut...supporting

confidence: 91%

“…This result supports our hypothesis that many microorganisms evolve to be non-autonomous genotypes but maintain abilities to perform one or multiple steps of metabolic pathways. These microorganisms presumably form MCFRs for the highly efficient degradation of hydrocarbons, a process that has been reported for several natural microbial communities [22][23][24]…”

Section: Species Exhibiting Metabolic Versatility While Being Non-aut...mentioning

confidence: 89%

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

Fang

Chen

Yuan

et al. 2023

Preprint

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In microbial systems, a metabolic pathway can be either completed by one autonomous population or alternatively be distributed among a consortium performing metabolic division of labor (MDOL), where several specialized populations cooperate to complete the pathway. MDOL facilitates the system's function by reducing the metabolic burden; however, it may also hinder the function by reducing the exchange efficiency of metabolic intermediates among individuals. As a result, the metabolic efficiency of a community is influenced by trade-offs between the metabolic specialization and versatility of individuals, with the latter potentially introducing metabolic redundancy into the community. However, it remains unclear how metabolic specialization and versatility of the individuals involved can be controlled in order to optimize the function of the community. In this study, we deconstructed the metabolic pathway of naphthalene degradation into four specialized steps and introduced them individually or combinatorically into different strains, with varying levels of metabolic specialization. Using these strains, we engineered 1,456 synthetic consortia with varying levels of metabolic redundancy and tested their naphthalene degradation efficiency. We found that 74 consortia possessing metabolic redundancy exhibited higher degradation efficiency than both the autonomous population and the rigorous MDOL community. Quantitative modeling derived from our experiments provides general strategies for identifying the most effective MDOL consortium with functional redundancy (MCFR) from a range of possible MCFRs. Our large-scale genomic analysis suggests that natural communities for hydrocarbon degradation are mostly functionally redundant. In summary, our study provides critical insights into the engineering of high-performance microbial systems and explains why functional redundancy is prevalent in natural microbial communities.

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Section: Species Exhibiting Metabolic Versatility While Being Non-aut...supporting

confidence: 91%

Section: Species Exhibiting Metabolic Versatility While Being Non-aut...mentioning

confidence: 89%

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

Fang

Chen

Yuan

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…Moreover, some of these patterns were also observed in the differential abundance analysis, which shows how Proteobacteria is the phylum whose families changed the most, which could be caused by the TPHs' variations (Vivas et al, 2008;Sutton et al, 2013;Gałązka et al, 2018). The analysis also highlights how families with known hydrocarbon degrading potential, like Alcaligenaceae or Pseudomonadaceae (Ruiz et al, 2021), displayed remarkable log2FoldChange values in December 2019, when TPHs' numbers were high. Conversely, ASVs from families of the phyla Acidobacteriota, and some Actinobacteriota or Firmicutes, appeared at the end of the process, when there were substantially less pollutants than at the beginning of the bioremediation process.…”

Section: Discussionmentioning

confidence: 73%

Field scale biodegradation of total petroleum hydrocarbons and soil restoration by Ecopiles: microbiological analysis of the process

et al. 2023

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Ecopiling is a method for biodegradation of hydrocarbons in soils. It derives from Biopiles, but phytoremediation is added to biostimulation with nitrogen fertilization and bioaugmentation with local bacteria. We have constructed seven Ecopiles with soil heavily polluted with hydrocarbons in Carlow (Ireland). The aim of the study was to analyze changes in the microbial community during ecopiling. In the course of 18 months of remediation, total petroleum hydrocarbons values decreased in 99 and 88% on average for aliphatics and aromatics, respectively, indicating a successful biodegradation. Community analysis showed that bacterial alfa diversity (Shannon Index), increased with the degradation of hydrocarbons, starting at an average value of 7.59 and ending at an average value of 9.38. Beta-diversity analysis, was performed using Bray-Curtis distances and PCoA ordination, where the two first principal components (PCs) explain the 17 and 14% of the observed variance, respectively. The results show that samples tend to cluster by sampling time instead of by Ecopile. This pattern is supported by the hierarchical clustering analysis, where most samples from the same timepoint clustered together. We used DSeq2 to determine the differential abundance of bacterial populations in Ecopiles at the beginning and the end of the treatment. While TPHs degraders are more abundant at the start of the experiment, these populations are substituted by bacterial populations typical of clean soils by the end of the biodegradation process. Similar results are found for the fungal community, indicating that the microbial community follows a succession along the process. This succession starts with a TPH degraders or tolerant enriched community, and finish with a microbial community typical of clean soils.

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“…However, petroleum-contaminated environments constitute rich reservoirs of microbial populations with hydrocarbon-catabolic abilities. Indeed, oil contamination favors the expansion of microorganisms capable of degrading these compounds through synergetic actions and cooperative relationships [ 8 , 9 ]. Hence, as chronically oil-stressed areas, soils from auto mechanic workshops (SAW) represent a valuable source of microorganisms with the ability to break down hydrocarbon contaminants and therefore be used in bioremediation strategies [ 5 , 8 , 10 , 11 ].…”

Section: Introductionmentioning

confidence: 99%

Use of Shotgun Metagenomics to Assess the Microbial Diversity and Hydrocarbons Degrading Functions of Auto-Mechanic Workshops Soils Polluted with Gasoline and Diesel Fuel

et al. 2023

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Bioaugmentation is a valuable technique for oil recovery. This study investigates the composition and functions of microbial communities in gasoline- and diesel-contaminated soils of garages Matoko (SGM) and Guy et Paul (SGP) originating from auto mechanic workshops as well as the concentration of soil enzymes β-glucosidase, β-glucosaminidase, and acid phosphatase. The work aimed to evaluate the presence of petroleum-hydrocarbon-degrading bacteria for the development of foreseen bioremediation of oil-contaminated soils. Microbial diversity, as given by shotgun metagenomics, indicated the presence of 16 classes, among which Actinobacteria and Gammaproteobacteria dominated, as well as more than 50 families, including the dominant Gordoniaceae (26.63%) in SGM and Pseudomonadaceae (57.89%) in SGP. The dominant bacterial genera in the two soils were, respectively, Gordonia (26.7%) and Pseudomonas (57.9%). The exploration of the bacterial metabolic abilities using HUMANn2 allowed to detect genes and pathways involved in alkanes and aromatic hydrocarbons in the two contaminated soils. Furthermore, enzymes β-glucosidase, β-glucosaminidase, and acid phosphatase were found in high concentrations ranging between 90.27 ± 5.3 and 804.17 ± 20.5 µg pN/g soil/h, which indicated active microbial metabolism. The high diversity of microorganisms with a hydrocarbon degradation genetic package revealed that the bacteria inhabiting the two soils are likely good candidates for the bioaugmentation of oil-contaminated soils.

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Metagenomic characterization reveals complex association of soil hydrocarbon-degrading bacteria

Cited by 22 publications

References 51 publications

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

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

Field scale biodegradation of total petroleum hydrocarbons and soil restoration by Ecopiles: microbiological analysis of the process

Use of Shotgun Metagenomics to Assess the Microbial Diversity and Hydrocarbons Degrading Functions of Auto-Mechanic Workshops Soils Polluted with Gasoline and Diesel Fuel

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