The bacterium Burkholderia cepacia (synonym Pseudomonas cepacia) was initially described in 1950 as the causal agent of onion sour skin (Burkholder, 1950). Over the years, strains phenotypically similar obtained from diverse ecological niches were classified as B. cepacia (Coenye et al., 2001). These strains were posteriorly reclassified at five distinct genomic species, which used to be referred to as the B. cepacia complex (Bcc) (Vandamme,’“, P., Holmes, ” B., Vancanneyt, M., Coenye, ’ T., Hoste, ’ B., Coopman, ’ R., Revets, ’ H., Lauwers, S., Gillis, ’ M., Kersters,’ And, K., Govan6, J.R.W., 1997). Nowadays, Bcc is composed of a versatile group of 26 closely related species (Martina et al., 2018, Morales-Ruíz et al., 2022), which may be satisfactorily identified using multilocus sequence analysis (MLSA) with housekeeping genes (Baia et al., 2021, Peeters et al., 2013, Tsuji and Kadota, 2020) and genomic studies (Santos and los., 2018, Vanlaere et al., 2009, Wallner et al., 2019).Fig 1.

Although most studies about the diversity of Bcc species have been carried out with strains obtained from clinical environments and environmental samples (Coenye et al., 2001, Jin et al., 2020, Martina et al., 2018, Mullins and Mahenthiralingam, 2021, Peeters et al., 2013, Spilker et al., 2009, Vandamme, 1997, Vanlaere et al., 2009); the knowledge about the diversity of Bcc species causing onion sour skin has been improved, and other species beyond B. cepacia have also been associated with this disease in the last number of years (Baia et al., 2021, Oliveira et al., 2017, Oliveira et al., 2019, Tsuji and Kadota, 2020). In this context; strains of B. cepacia, B. cenocepacia, B. ambifaria, and B. pyrrocinia have been recently associated with the rot of onion bulbs in Japan (Tsuji and Kadota, 2020); where this disease was reported in 2001 (Sotokawa and Takikawa, 2004). Since 2015; strains of the Bcc have also been identified in the main onion-producing regions of north-east Brazil (Oliveira et al., 2017, Oliveira et al., 2019); and MLSA with housekeeping genes have revealed the predominance of lineages of B. cenocepacia causing onion sour skin (Baia et al., 2021).

Among Bcc species associated with the rot of onion bulbs, B. cenocepacia stands out because it behaves as a genetically heterogeneous group composed of at least four phylogenetic lineages (IIIA, IIIB, IIIC, and IIID), which have been identified using recA gene sequencing (Mahenthiralingam et al., 2000, Vandamme et al., 2003). The lineages IIIA and IIIB have been found both in clinical isolates (Wallner et al., 2019) and causing onion sour skin (Baia et al., 2021), while lineages IIIC and IIID have been detected exclusively in soil and human clinical settings, respectively (Vandamme et al., 2003). Based on comparisons among genomes of strains from lineages IIIA and IIIB, it was recently proposed that strains from the former lineage should be classified as B. cenocepacia sensu stricto. In contrast, strains from the latter lineage were reclassified as B. servocepacia (Wallner et al., 2019). However, according to Morales-Ruíz et al. (Morales-Ruíz et al., 2022), this epithet could not be validated due to being in disagreement concerning the rules for describing new species contained in the International Code of Nomenclature of Prokaryotes (ICNP) (Parker et al., 2008), showing errors in the type strain name and the protologue describing the novel species. Thus, aiming to validate the taxonomic status of this species by providing information that agrees with the criteria defined by ICNP, it was proposed that “B. servocepacia” be classified as Burkholderia orbicola (Morales-Ruíz et al., 2022). In turn, the high percentage of divergence of the concatenated sequence of the seven housekeeping genes (recA, gyrB, atpD, gltB, lepA, phaC, and trpB) has indicated that lineages IIIC and IIID may be distinct species. This hypothesis is reinforced because the lineage IIID and B. contaminans have shown a low divergence percentage, suggesting they may be synonymous (Baia et al., 2021). In addition, phylogenomics and taxogenomics analyses of strains misidentified and/or unidentified showed the presence of species closely related to B. cenocepacia and B. orbicola that have not been characterized yet (Jin et al., 2020, Mullins and Mahenthiralingam, 2021), which needs to be further studied.

Recently, two putative novel B. cenocepacia lineages were found causing onion sour skin in the semi-arid region of north-east Brazil (Baia et al., 2021). However, their taxonomic status has not yet been elucidated. Therefore, this study aimed to investigate the taxonomic position of these putative novel lineages using a taxogenomic approach to classify them appropriately within the Bcc. Thus, we used type (strain) genome server (TYGS), average nucleotide identity (ANI) values, tetranucleotide frequency correlation coefficients (TETRA), digital DNA–DNA hybridization (dDDH) values, and phylogenomic analysis to classify these lineages as two novel species, namely: Burkholderia semiarida sp. nov. and B. sola sp. nov.