Abstract
Alcaligenes aquatilis QD168 is a marine, aromatic hydrocarbon-degrading bacterium, isolated from an oil-polluted sediment of Quintero Bay, an industrial-coastal zone that has been chronically impacted by diverse pollutants. The aims of this study were to characterize the phylogenomic positions of Alcaligenes spp. and to characterize the genetic determinants and the physiological response of A. aquatilis QD168 to model environmental stressors (benzene, oxidizing agents, and salt). Phylogenomic analyses, using 35 housekeeping genes, clustered A. aquatilis QD168 with four other strains of Alcaligenes spp. (A. aquatilis BU33N, A. faecalis JQ135, A. faecalis UBA3227, and A. faecalis UBA7629). Genomic sequence analyses of A. aquatilis QD168 with 25 Alcaligenes spp., using ANIb, indicated that A. aquatilis BU33N is the closest related strain, with 96.8% ANIb similarity. Strain QD168 harbors 95 genes encoding proteins of seven central catabolic pathways, as well as sixteen peripheral catabolic pathways/reactions for aromatic compounds. A. aquatilis QD168 was able to grow on 3-hydroxybenzoate, 4-hydroxybenzoate, benzoate, benzene, 3-hydroxycinnamate, cinnamate, anthranilate, benzamide, 4-aminobenzoate, nicotinate, toluene, biphenyl and tryptophan, as sole carbon or nitrogen source. Benzene degradation was further analyzed by growth, metabolite identification and gene expression analyses. Benzene strongly induced the expression of the genes encoding phenol hydroxylase (dmpP) and catechol 1,2-dioxygenase (catA). Additionally, 30 genes encoding transcriptional regulators, scavenging enzymes, oxidative damage repair systems and isozymes involved in oxidative stress response were identified. Oxidative stress response of strain QD168 to hydrogen peroxide and paraquat was characterized, demonstrating that A. aquatilis QD168 is notably more resistant to paraquat than to H2O2. Genetic determinants (47 genes) for osmoprotective responses were identified, correlating with observed high halotolerance by strain QD168. The physiological adaptation of A. aquatilis QD168 to environmental stressors such as pollutants, oxidative stress and salinity may be exploited for bioremediation of oil-polluted saline sites.
Highlights
The Alcaligenes genus, belonging to the Alcaligenaceae family of the order Burkholderiales (Garrity et al, 2005), was first described in 1911 during the study of a bacterium isolated from a fecal sample and identified as A. faecalis (Kühnemann, 1911)
To investigate the phylogenomic relationships of strains of Alcaligenes spp., a more comprehensive set of housekeeping gene markers was obtained from strain QD168 and 25 publicly available genomes of Alcaligenes spp. (Supplementary Table S1), to perform a multi-locus sequence analysis (MLSA)
Genomes corresponding to the Alcaligenes genus were highly represented by the species, A. faecalis, comprising approximately 84.6% of all genomes of Alcaligenes spp. analyzed
Summary
The Alcaligenes genus, belonging to the Alcaligenaceae family of the order Burkholderiales (Garrity et al, 2005), was first described in 1911 during the study of a bacterium isolated from a fecal sample and identified as A. faecalis (Kühnemann, 1911). Strains of Alcaligenes spp. have been isolated from diverse environments, such as water (Regar et al, 2016), agricultural soil (Liu et al, 2016), crude oil-polluted sites (Singha et al, 2017), industrial processes (Qiu et al, 2017; Basharat et al, 2018), insects (Quiroz-Castañeda et al, 2015) and human clinical samples (Winslow et al, 1920; Al Laham et al, 2017). Phenolicus MB207 and 10 other strains of Alcaligenes spp. identified biosynthetic clusters for butyrolactone, ectoine, resorcinol, terpene, non-ribosomal peptides and polyketide synthases (Basharat et al, 2018). Four complete genome sequences are publicly available for this genus, including those of A. faecalis ZD02 (Ju et al, 2016), A. faecalis DSM 30030T (Genome accession: GCA_002443155.1), A. faecalis JQ135 (Zhang et al, 2018) and A. faecalis P156 (Genome accession: GCA_001641975.2), but no whole-genome bioprospecting analyses have been performed previously for any of these strains
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