Properties of Modestobacter deserti sp. nov., a Kind of Novel Phosphate-Solubilizing Actinobacteria Inhabited in the Desert Biological Soil Crusts

Abstract

Three Gram-stain-positive, aerobic, motile actinobacterial strains designated as CPCC 205119^T, CPCC 205215, and CPCC 205251 were isolated from different biological soil crust samples collected from Tengger Desert, China. The 16S rRNA gene sequence comparison of these three strains showed they had almost identical 16S rRNA genes, which were closely related to members of the family Geodermatophilaceae, with the highest similarities of 96.3-97.3% to the species of Modestobacter. In the phylogenetic tree based on 16S rRNA gene sequences, these isolates clustered into a subclade next to the branch containing the species of Modestobacter lapidis and Modestobacter multiseptatus, within the lineage of the genus Modestobacter. The comparative genomic characteristics (values of ANI, dDDH, AAI, and POCP) and the phenotypic properties (morphological, physiological, and chemotaxonomic characteristics) of these isolates readily supported to affiliate them to the genus Modestobacter as a single separate species. For which, we proposed that the isolates CPCC 205119^T, CPCC 205215, and CPCC 205251 represent a novel species of the genus Modestobacter as Modestobacter deserti sp. nov. CPCC 205119^T (=I12A-02624=NBRC 113528^T=KCTC 49201^T) is the type strain. The genome of strain CPCC 205119^T consisted of one chromosome (4,843,235bp) containing 4,424 coding genes, 48 tRNA genes, five rRNA genes, three other ncRNA genes, and 101 pseudogenes, with G+C content of 74.7%. The whole-genome sequences analysis indicated that this species contained alkaline phosphatase genes (phoA/phoD), phosphate transport-related genes (phoU, phnC, phnD, phnE, phoB, phoH, phoP, phoR, pitH, ppk, pstA, pstB, pstC, and pstS), trehalose-phosphate synthase gene (otsA), trehalose 6-phosphate phosphatase gene (otsB) and other encoding genes for the properties that help the microorganisms to adapt to harsh environmental conditions prevalent in deserts. Strains of this species could solubilize tricalcium phosphate [Ca₃(PO₄)₂] and phytin, assimilate pyrophosphate, thiophosphate, dithiophosphate, phosphoenol pyruvate, 2-deoxy-d-glucose-6-phosphate, and cysteamine-S-phosphate.

Keywords: Modestobacter deserti; average nucleotide identity; biological soil crusts; genotype; pan-genome; phenotype.

Figure 1

Neighbour-joining tree based on 16S rRNA gene sequences showing the relationship of the strains CPCC 205119^T, CPCC 205215, and CPCC 205251 with representatives of the family Geodermatophilaceae. Filled circles indicate that the corresponding nodes were also recovered in the trees generated with the maximum-likelihood and maximum-parsimony methods. Bootstrap values (>50%) are shown as percentages of 1,000 replicates. Bar, 1nt substitutions per 100nt.

Figure 2

Heatmap of putative stress-responding genes predicted in the genomes of strains CPCC 205119^T, CPCC 205215, CPCC 205251, and their closest phylogenic neighbors according to the copy number of the genes from the Rapid Annotation using Subsystem Technology (RAST) annotation.

Figure 3

Overview of the pan-genome generated by Bacterial Pan-genome Analysis (BPGA) using three strains of the species Modestobacter deserti. (A) The gene family frequency spectrum. (B) The pan genome profile trends of the species Modestobacter deserti obtained using clustering tools USEARCH.

Figure 4

The assigned metabolic pathways associated with the core, accessory, and unique genes among the species Modestobacter deserti from the KEGG database.

Figure 5

Transmission electron micrograph of strain CPCC 205119^T grown on GYM semi-solid medium (0.3% agar) for 7days at 28°C. Bar, 2μm. (A) Showing the flagella; (B) arrow, indicating the bud-like structure.