Paenarthrobacter sp. GOM3 Is a Novel Marine Species With Monoaromatic Degradation Relevance

Abstract

Paenarthrobacter sp. GOM3, which is a strain that represents a new species-specific context within the genus Paenarthrobacter, is clearly a branched member independent of any group described thus far. This strain was recovered from marine sediments in the Gulf of Mexico, and despite being isolated from a consortium capable of growing with phenanthrene as a sole carbon source, this strain could not grow successfully in the presence of this substrate alone. We hypothesized that the GOM3 strain could participate in the assimilation of intermediate metabolites for the degradation of aromatic compounds. To date, there are no experimental reports of Paenarthrobacter species that degrade polycyclic aromatic hydrocarbons (PAHs) or their intermediate metabolites. In this work, we report genomic and experimental evidence of metabolic benzoate, gentisate, and protocatechuate degradation by Paenarthrobacter sp. GOM3. Gentisate was the preferred substrate with the highest volumetric consumption rate, and genomic analysis revealed that this strain possesses multiple gene copies for the specific transport of gentisate. Furthermore, upon analyzing the GOM3 genome, we found five different dioxygenases involved in the activation of aromatic compounds, suggesting its potential for complete remediation of PAH-contaminated sites in combination with strains capable of assimilating the upper PAH degradation pathway. Additionally, this strain was characterized experimentally for its pathogenic potential and in silico for its antimicrobial resistance. An overview of the potential ecological role of this strain in the context of other members of this taxonomic clade is also reported.

Keywords: Gulf of Mexico; aromatic compounds; bioprospection; hydrocarbon-degrading bacteria; marine bacteria.

FIGURE 1

Phylogenomic unrooted tree inferred with 92 housekeeping bacterial core genes in the UBCG pipeline. Gene support indices (GSIs) are represented in color scale per node. Bar 0.05 substitution per site. The Micrococcus terreus CGMCC 1.7054^T genome was used as an outgroup.

FIGURE 2

Metabolic completeness of C, O, N, S, and Fe cycles of strains related to pangenomic analysis. The most complete pathways in biogeochemical cycles are marked in red, and the least complete pathways shift to blue. P. ureafaciens^a corresponds to RefSeq assembly accession GCF_006538985, and P. aurescens^b corresponds to RefSeq assembly accession GCF_004028095.

FIGURE 3

Genomic and experimental evidence of aromatic compound degradation by Paenarthrobacter sp. GOM3. Degradation pathways and genomic context are shown for three aromatic compounds: (A) benzoate, (B) gentisate, and (C) protocatechuate. (D) Growth kinetics and decrease in its corresponding compound concentration. Whiskers represent the standard deviation of three biological replicates. Metabolic compounds: (1) benzoate; (2) cis-1,2-dihydroxycyclohexa-3,5-diene-1-carboxylate; (3) catechol; (4) cis,cis-muconate; (5) (+)-muconolactone; (6) 3-oxoadipate enol-lactone; (7) 3-hydroxybenzoate; (8) gentisate; (9) 3-maleylpyruvate; (10) 3-fumarylpyruvate; (11) fumarate; (12) pyruvate; (13) protocatechuate; (14) beta-carboxy-cis,cis-muconate; (15) gamma-carboxymuconolactone; (16) 3-oxoadipate; (17) 3-oxoadipyl-CoA; and (18) succinyl-CoA. Concentrations of each aromatic compound in abiotic controls in gray.

FIGURE 4

Substrate decrease and growth kinetics of Paenarthrobacter sp. GOM3 in the presence of different mixtures of aromatic compounds (A) benzoate and gentisate, (B) benzoate and protocatechuate, (C) gentisate and protocatechuate and (D) the three compounds. Whiskers represent the standard deviation of three biological replicates. Aromatic compound in abiotic controls in gray.