Delineation of a Subgroup of the Genus Paraburkholderia, Including P. terrae DSM 17804(T), P. hospita DSM 17164(T), and Four Soil-Isolated Fungiphiles, Reveals Remarkable Genomic and Ecological Features—Proposal for the Definition of a P. hospita Species Cluster

The fungal-interactive (fungiphilic) strains BS001, BS007, BS110, and BS437 have previously been preliminarily assigned to the species Paraburkholderia terrae. However, in the (novel) genus Paraburkholderia, an as-yet unresolved subgroup exists, that clusters around Paraburkholderia hospita (containing the species P. terrae, P. hospita, and Paraburkholderia caribensis). To shed light on the precise relationships across the respective type strains and the novel fungiphiles, we here compare their genomic and ecophysiological features. To reach this goal, the genomes of the three type strains, with sizes ranging from 9.0 to 11.5 Mb, were de novo sequenced and the high-quality genomes analyzed. Using whole-genome, ribosomal RNA and marker-gene-concatenate analyses, close relationships between P. hospita DSM 17164(T) and P. terrae DSM 17804(T), versus more remote relationships to P. caribensis DSM 13236(T), were found. All four fungiphilic strains clustered closely to the two-species cluster. Analyses of average nucleotide identities (ANIm) and tetranucleotide frequencies (TETRA) confirmed the close relationships between P. hospita DSM 17164(T) and P. terrae DSM 17804(T) (ANIm = 95.42; TETRA = 0.99784), as compared with the similarities of each one of these strains to P. caribensis DSM 13236(T). A species cluster was thus proposed. Furthermore, high similarities of the fungiphilic strains BS001, BS007, BS110, and BS437 with this cluster were found, indicating that these strains also make part of it, being closely linked to P. hospita DSM 17164(T) (ANIm = 99%; TETRA = 0.99). We propose to coin this cluster the P. hospita species cluster (containing P. hospita DSM 17164(T), P. terrae DSM 17804(T), and strains BS001, BS007, BS110, and BS437), being clearly divergent from the closely related species P. caribensis (type strain DSM 13236(T)). Moreover, given their close relatedness to P. hospita DSM 17164(T) within the cluster, we propose to rename the four fungiphilic strains as members of P. hospita. Analysis of migratory behavior along with fungal growth through soil revealed both P. terrae DSM 17804(T) and P. hospita DSM 17164(T) (next to the four fungiphilic strains) to be migration-proficient, whereas P. caribensis DSM 13236(T) was a relatively poor migrator. Examination of predicted functions across the genomes of the seven investigated strains, next to several selected additional ones, revealed the common presence of features in the P. hospita cluster strains that are potentially important in interactions with soil fungi. Thus, genes encoding specific metabolic functions, biofilm formation (pelABCDEFG, pgaABCD, alginate-related genes), motility/chemotaxis, type-4 pili, and diverse secretion systems were found.