Reclassification of the Specialized Metabolite Producer Pseudomonas mesoacidophila ATCC 31433 as a Member of the Burkholderia cepacia Complex

Abstract

Pseudomonas mesoacidophila ATCC 31433 is a Gram-negative bacterium, first isolated from Japanese soil samples, that produces the monobactam isosulfazecin and the β-lactam-potentiating bulgecins. To characterize the biosynthetic potential of P. mesoacidophila ATCC 31433, its complete genome was determined using single-molecule real-time DNA sequence analysis. The 7.8-Mb genome comprised four replicons, three chromosomal (each encoding rRNA) and one plasmid. Phylogenetic analysis demonstrated that P. mesoacidophila ATCC 31433 was misclassified at the time of its deposition and is a member of the Burkholderia cepacia complex, most closely related to Burkholderia ubonensis. The sequenced genome shows considerable additional biosynthetic potential; known gene clusters for malleilactone, ornibactin, isosulfazecin, alkylhydroxyquinoline, and pyrrolnitrin biosynthesis and several uncharacterized biosynthetic gene clusters for polyketides, nonribosomal peptides, and other metabolites were identified. Furthermore, P. mesoacidophila ATCC 31433 harbors many genes associated with environmental resilience and antibiotic resistance and was resistant to a range of antibiotics and metal ions. In summary, this bioactive strain should be designated B. cepacia complex strain ATCC 31433, pending further detailed taxonomic characterization.IMPORTANCE This work reports the complete genome sequence of Pseudomonas mesoacidophila ATCC 31433, a known producer of bioactive compounds. Large numbers of both known and novel biosynthetic gene clusters were identified, indicating that P. mesoacidophila ATCC 31433 is an untapped resource for discovery of novel bioactive compounds. Phylogenetic analysis demonstrated that P. mesoacidophila ATCC 31433 is in fact a member of the Burkholderia cepacia complex, most closely related to the species Burkholderia ubonensis. Further investigation of the classification and biosynthetic potential of P. mesoacidophila ATCC 31433 is warranted.

Total Syntheses of Bulgecins A, B, and C and Their Bactericidal Potentiation of the β-Lactam Antibiotics

“…Each is a simple variation on a glycosylated iminosaccharide, and each is biosynthesized by a Gram-negative bacterium (annotated then as Pseudomonas mesoacidophilia but recently reassigned as Paraburkholderia acidophila ). 13,14 Additional studies with this bacterium by Asai and co-workers led to the isolation of a monobactam-class β-lactam antibiotic, sulfazecin ( 4 ). 15,16 The combination of bulgecin (itself bereft of antibacterial activity) with sulfazecin significantly improved the latter’s antibacterial activity toward other Gram-negative bacteria.…”

Pseudomonas putidachromosomal toxin-antitoxin systems carry neither clear fitness benefits nor big costs

“…To test this, distribution and diversity of 13 P. putida TA loci in genus Pseudomonas was analysed by searching 334 fully sequenced Pseudomonas strains available in Pseudomonas genome database 47 for putative homologs (Figure S1). Pseudomonas mesoacidophila ATCC 31422 was omitted from the analysis as this bacterium was recently reclassified as a member of Burkholderia cepacia complex 48 . We first searched for homologs of P. putida KT2440 (isogenic to PaW85) antitoxins and found that their distribution in other Pseudomonads highly depends on the particular TA system.…”

Genome-based taxonomic classification

“…Number of whole genome sequencing projects has surged at an unprecedented momentum and is expected to gather pace since the current number of complete genomes represent only a tiny fraction of the total number of bacterial species on this planet. Over the years, number of studies have highlighted large scale genetic variations at intra-species level and this has led to reclassification of several bacterial species (Stropko et al 2014;Lawson et al 2016;Vincent et al 2016;Kook et al 2017;Loveridge et al 2017;Liu et al 2018). This scenario might arise if the species delineation is based only on the traditional methodology followed for the species identification or due to outsourcing the genome sequencing and assembly to other service providers.…”

“…Recently, several bacterial species have been reclassified based on the gANI analysis (Godoy et al 2003;Stropko et al 2014;Lawson et al 2016;Vincent et al 2016;Kook et al 2017;Loveridge et al 2017;Sant'Anna et al 2017;Liu et al 2018). In an earlier study, Biller et al (2014) observed remarkable sequence diversity among 27 different Prochlorococcus strains from diverse oceanic regions with wide variation in their GC% (30.8-50.6), and these strains were further grouped under physiologically distinct phylogenetic clades.…”