Actinospongicola halichondriae gen. nov. sp. nov., the first sponge-derived cultivated representative of a new genus within the class Acidimicrobiia

A new strain (named Hal317T) of the family Iamiaceae within the class Acidimicrobiia was isolated from the marine breadcrumb sponge Halichondria panicea sampled in the Kiel Fjord (Baltic Sea, Germany). This strain is one of the few isolates of the class Acidimicrobiia, which is under-represented in cultivation efforts and comprises only 16 validly described species. Because strain Hal317T showed a small translucent colony morphology, it can easily be overlooked on agar plates. Phylogenetic analysis of the full-length 16S rRNA gene sequence revealed similarities from 84.86 - 91.54% to all known type strains of the class Acidimicrobiia. The phylogenetic analysis of the 16S rRNA gene sequences depicted a cluster of strain Hal317T with its closest relative Aquihabitans daechungensis CH22-21T (90.94%) which was also observed by genome phylogeny. Genome comparisons of strain Hal317T with type strains of the family Iamiaceae exhibited average nucleotide identities <71.49% and digital DNA-DNA hybridization values <70%. Strain Hal317T exhibited features of a sponge-associated life-style based on genome predictions, e.g. metabolisation of diverse carbohydrates derived from sponge, transport of glutamate, participation of sulfur, nitrogen and phosphorus cycle in sponge environments, as well as synthesis of vitamins. Moreover, stress response-related genes involved in ectoine synthesis, defense mechanisms against reactive oxygen species (ROS), chaperones, and toxin antitoxin systems were shown in the genome of strain Hal317T. Within the family Iamiaceae strain Hal317T revealed unique genomic features such as a substrate-specific phosphonate pathway, a glutamate-uptake system, a non-phosphorylated L-fucose pathway, and extracellular proteases. Strain Hal317T was determined to be microaerophilic and sea salt-dependent. Optimal growth occurred at 30 - 35 °C, within a salinity range of 1 - 2% sea salt, and a pH range between 6 - 7. The major fatty acids identified were C18:1 ω7c, C16:1 ω7c, C17:1 ω8c, and C16:0. Whole-cell sugar analysis revealed rhamnose, ribose, mannose, and galactose. Meso-diaminopimelic acid was observed in the whole-cell hydrolysate. The major respiratory menaquinone was MK-9(H8) with minor amounts of MK-9(H6) and MK-9(H10). The polar lipid profile comprised diphosphatidylglycerol, a glycophospholipid, two glycolipids, four phospholipids, and an unknown lipid. The DNA G+C content of strain Hal317T was 68.70 mol%. Based on the polyphasic approach, strain Hal317T could be distinguished from known genera of the family Iamiaceae, and we propose the name Actinospongicola halichondriae gen. nov., sp. nov. The type strain is Hal317T (= DSM 114536T = LMG 32795T). Our study sheds light on the Acidimicrobiia which is typical of few representatives and difficult to isolate. Additionally, the new sponge-derived isolate offers valuable insights into the host-bacteria association.