Genomic and phylogenomic insights into the family Streptomycetaceae lead to the proposal of six novel genera

Abstract

The family Streptomycetaceae is a large and diverse family within the phylum Actinomycetota . The members of the family are known for their ability to produce medically important secondary metabolites, notably antibiotics. In this study, 19 type strains showing low 16S rRNA gene similarity (<97.3 %) to other members of the family Streptomycetaceae were identified and their high genetic diversity was reflected in a phylogenomic analysis using conserved universal proteins. This analysis resulted in the identification of six distinct genus-level clades, with two separated from the genus Streptacidiphilus and four separated from the genus Streptomyces . Compared with members of the genera Streptacidiphilus and Streptomyces , average amino acid identity (AAI) analysis of the novel genera identified gave values within the range of 63.9–71.3 %, as has been previously observed for comparisons of related but distinct bacterial genera. The whole-genome phylogeny was reconstructed using PhyloPhlAn 3.0 based on an optimized subset of conserved universal proteins, the results of AAI and percentage of conserved proteins (POCP) analyses indicated that these phylogenetically distinct taxa may be assigned to six novel genera, namely Actinacidiphila gen. nov., Mangrovactinospora gen. nov., Peterkaempfera gen. nov., Phaeacidiphilus gen. nov., Streptantibioticus gen. nov. and Wenjunlia gen. nov.

Generation of a high quality library of bioactive filamentous actinomycetes from extreme biomes using a culture-based bioprospecting strategy

“…Twenty-two (19.1%) of representative isolates found to belong to putatively novel species were assigned to genera other than Streptomyces . Nearly half of them were most closely related to the type strains of Streptomyces species that were transferred to the genus Actinacidiphila , namely A. alni, A. bryophytorum, A, paucisporea, A. rubida , and A. yanglinensis ( Madhaiyan et al, 2022 ) whereas others were most closely related to three validly named Streptacidiphulus species, S. albus ( Kim et al, 2003 ), S. carbonis ( Kim et al, 2003 ) and S. hamsterleyensis ( Golińska et al, 2013 ). It seems likely that presumptively novel isolates shown to be most closely related to the type strains of Streptomyces cocklensis ( Kim et al, 2012 ) and Streptomyces ferralitis ( Saintpierre-Bonaccio et al, 2004 ) will be found to belong to the genus Actinacidiphila given the close phylogenetic relationships of these taxa with Streptomyces species recently transferred to this genus ( Labeda et al, 2012 , 2017 ).…”

“…Streptomycetes remain a rich source of new specialised metabolites, especially antibiotics ( Sivalingam et al, 2019 ; Lacey and Rutledge, 2022 ) with the promise of more to come now that improved analytical procedures, such as genome mining and genetic engineering, are opening up new opportunities for drug discovery ( Luo et al, 2014 ; Atanasov et al, 2021 ). However, the search for new natural products from streptomycetes using culture-dependent strategies needs to be tailored to meet developments in their ecology and systematics ( Nouioui et al, 2018 ; Traxler and Rozen, 2022 ; Wang et al, 2022 ), as shown by the transfer of validly named acidotolerant and acidophilic Streptomyces species to the genera Actinacidiphila, Streptantibioticus and Wenjunlia whilst some Streptacidiphilus species have been moved to form the new genera Peterkaempfera and Phaeacidiphilus ( Madhaiyan et al, 2022 ). Members of these poorly studied taxa are promising sources of new bioactive compounds ( Golińska et al, 2023 ), as are Kitasatospora strains ( Takahashi, 2017 ) which also belong to the family Streptomycetaceae .…”

Streptantibioticus silvisoli sp. nov., acidotolerant actinomycetes from pine litter, reclassification of Streptomyces cocklensis, Streptomyces ferralitis, Streptomyces parmotrematis and Streptomyces rubrisoli as Actinacidiphila cocklensis comb. nov., Streptantibioticus ferralitis comb. nov., Streptantibioticus parmotrematis comb. nov. and Streptantibioticus rubrisoli comb. nov., and emended descriptions of the genus Streptantibioticus, the family Streptomycetaceae and Streptomyces iconiensis

“…The PCR products were purified using a purification kit (Qiagen), according to the manufacturer’s instructions and the concentration and quality of each of the purified PCR products were checked using a Nanodrop spectrophotometer (NanoDrop 2000, Thermo Fisher Scientific) and by gel electrophoresis using a 1 kb DNA ladder (Kapa Biosystems). The purified PCR products of the isolates were sequenced on an ABI 3730xl Genetic Analyzer (Applied Biosystems) at the Institute of Biochemistry and Biophysics of the Polish Academy of Sciences in Warsaw and the resultant sequences compared with corresponding sequences of the type strains of phylogenetically related Actinacidiphila and Streptomyces species and the type species of the other nine genera classified in the family Streptomycetaceae [6] using the EzbioCloud server [46] and then aligned using Clustal W [47].…”

“…It is also notable that S. cocklensis DSM 42063 T forms a well-supported lineage with A. bryophytorum DSM 42138 T , the type strain of A. paucisporea is closely associated with these organisms; the subclade encompassing these strains is underpinned by a 100 % bootstrap value. All of the type strains of the genera classified in the family Streptomycetaceae [6] formed distinct evolutionary lineages. Key genomic features of the isolates, Streptantibioticus cattleyicolor DSM 46488 T , Streptomyces ferralitis DSM 41836 T , S. parmotrematis NBRC 115203 T and S. rubrisoli DSM 42083 T , their closest phylogenomic neighbours, and the type strains of more remotely associated Streptomyces species are shown in Table 1.…”

“…It is evident from the MLSA and phylogenomic trees, the POCP data, and associated phenotypic properties that the isolates and the type strains of S. ferralitis [61], S. parmotrematis [30] and S. rubrisoli [62] are bona fide members of the family Streptomycetaceae [6,15]. It is also clear from the wealth of genomic, genotypic and phenotypic data that the isolates belong to a novel species which can be distinguished from its closest neighbour, S. parmotrematis NBRC 115203 T .…”