Paraburkholderia madseniana sp. nov., a phenolic acid-degrading bacterium isolated from acidic forest soil

Abstract

RP11T was isolated from forest soil following enrichment with 4-hydroxybenzoic acid. Cells of RP11T are aerobic, non-sporulating, exhibit swimming motility, and are rods (0.8 µm by 1.4 µm) that often occur as diplobacillus or in short chains (3–4 cells). Optimal growth on minimal media containing 4-hydroxybenzoic acid (µ=0.216 hr−1) occurred at 30 °C, pH 6.5 or 7.0 and 0% salinity. Comparative chemotaxonomic, genomic and phylogenetic analyses revealed the isolate was distinct from its closest relative type strains identified as Paraburkholderia aspalathi LMG 27731T, Paraburkholderia fungorum LMG 16225T and Paraburkholderia caffeinilytica CF1T. Strain RP11T is genetically distinct from P. aspalathi , its closest relative, in terms of 16S rRNA gene sequence similarity (98.7%), genomic average nucleotide identity (94%) and in silico DNA–DNA hybridization (56.7 %±2.8). The composition of fatty acids and substrate utilization pattern differentiated strain RP11T from its closest relatives, including growth on phthalic acid. Strain RP11T encoded the greatest number of aromatic degradation genes of all eleven closely related type strains and uniquely encoded a phthalic acid dioxygenase and paralog of the 3-hydroxybenzoate 4-monooxygenase. The only ubiquinone detected in strain RP11T was Q-8, and the major cellular fatty acids were C16 : 0, 3OH-C16 : 0, C17 : 0 cyclo, C19 : 0 cyclo ω8c, and summed feature 8 (C18 : 1 ω7c/ω6c). On the basis of this polyphasic approach, it was determined that strain RP11T represents a novel species from the genus Paraburkholderia for which the name Paraburkholderia madseniana sp. nov. is proposed. The type strain is RP11T (=DSM 110123T=LMG 31517T).

Phenolic acid-degradingParaburkholderiaprime decomposition in forest soil

“…Members of the family Burkholderiaceae are major zymogenous populations in soil [32] and the rapid in situ growth of RP11 ASV was evident in its increase from ~ 0.7% to 15% of total sequences in 24 hrs, during the period of maximal PHB respiration. Consistent with these observations, isolate RP11 T exhibited rapid growth in pure culture with PHB as the sole carbon source (µ = 0.22 hr -1 ), and encodes six copies of the rrn operon, characteristic of high growth rate capacity [63,84]. These results indicate that the microbial traits relevant to priming are partly defined by rapid growth, highlighting the importance of pulsed sources of phenolic C in SOC cycling.…”

“…Paraburkholderia are renowned for their oxidative catabolism of aromatics, phenolics, and polyaromatic hydrocarbons [87,88]. The two dominant PHB-degrading phylotypes in our study matched to P. madseniana and P. xenovorans, species which encode an extensive array of aromatic degrading pathways [52,63]. P. madseniana RP11 T encoded among the greatest number of aromatic degrading genes compared to close relatives, including several putatively secreted oxidases [76] and aryl-alcohol oxidases important for bacterial lignin degradation [40].…”

“…xenovorans LB400 T , species notable for having more genes and pathways associated with phenolic acid degradation than close relatives, and among the highest of any bacterial species [63,77]. These findings are inconsistent with the hypothesis that all priming phenomena result from the non-specific, aggregate activity of functionally and phylogenetically diverse microbial populations [45].…”

“…PHB degrading isolates were obtained from red pine and sugar maple LnC soil by serial dilution. Diluted cells were plated onto mineral salts media containing 3 mM PHB (MSM-PHB) as the sole carbon source and incubated at room temperature as previously described [63].…”

“…One of these strains, isolate RP11 T , was chosen for genome sequencing. The RP11 T genome was large (10.1 Mb), contained two chromosomes and encoded 6 copies of the rrn operon [63]. The genome encoded the complete pathway to mineralize PHB and included two paralogs of pobA which shared 48% amino acid sequence identity.…”