Comparative Genomics Reveals Genetic Diversity and Metabolic Potentials of the Genus Qipengyuania and Suggests Fifteen Novel Species

Abstract

Members of the genus Qipengyuania are heterotrophic bacteria frequently isolated from marine environments with great application potential in areas such as carotenoid production. However, the genomic diversity, metabolic function, and adaption of this genus remain largely unclear. Here, 16 isolates related to the genus Qipengyuania were recovered from coastal samples and their genomes were sequenced. The phylogenetic inference of these isolates and reference type strains of this genus indicated that the 16S rRNA gene was insufficient to distinguish them at the species level; instead, the phylogenomic reconstruction could provide the reliable phylogenetic relationships and confirm 15 new well-supported branches, representing 15 putative novel genospecies corroborated by the digital DNA-DNA hybridization and average nucleotide identity analyses. Comparative genomics revealed that the genus Qipengyuania had an open pangenome and possessed multiple conserved genes and pathways related to metabolic functions and environmental adaptation, despite the presence of divergent genomic features and specific metabolic potential. Genetic analysis and pigment detection showed that the members of this genus were identified as carotenoid producers, while some proved to be potentially aerobic anoxygenic photoheterotrophs. Collectively, the first insight into the genetic diversity and metabolic potentials of the genus Qipengyuania will contribute to better understanding of the speciation and adaptive evolution in natural environments. IMPORTANCE The deciphering of the phylogenetic diversity and metabolic features of the abundant bacterial taxa is critical for exploring their ecological importance and application potential. Qipengyuania is a genus of frequently isolated heterotrophic microorganisms with great industrial application potential. Numerous strains related to the genus Qipengyuania have been isolated from diverse environments, but their genomic diversity and metabolic functions remain unclear. Our study revealed a high degree of genetic diversity, metabolic versatility, and environmental adaptation of the genus Qipengyuania using comparative genomics. Fifteen novel species of this genus have been established using a polyphasic taxonomic approach, expanding the number of described species to almost double. This study provided an overall view of the genus Qipengyuania at the genomic level and will enable us to better uncover its ecological roles and evolutionary history.

Keywords: Qipengyuania; comparative genomics; genetic diversity; metabolic potentials; novel species description..

FIG 1

Phylogenetic trees of bacteria within the genus Qipengyuania respectively based on 16S rRNA gene sequences (a) and the Qipengyuania-specific core genes (b). The two trees are inferred using the maximum likelihood method. Type strain A. gangjinensis CGMCC 1.15024 (accession numbers EU428782 and CP018097) is used as an outgroup. The species names are effectively but not yet validly published and thus are in quotation marks. Bootstrap values greater than 50/80% are shown at branch points. Bar, 0.02/0.2 represents the number of substitutions per site.

FIG 2

The heatmap of dDDH values at the lower left and ANI values at the upper right (a), and the distribution of key metabolic genes and pathways among strains of the genus Qipengyuania (b). The dDDH and ANI values are visualized using the “Heatmap” tool of the TBtools. The key metabolic genes and pathways are annotated by RAST.

FIG 3

The pangenome analysis of bacteria within the genus Qipengyuania. (a) The numbers and proportions of core genes, accessory genes, and unique genes. (b) The boxplots of the pangenome (yellow) and core genome (cyan) of the 31 analyzed genomes. (c) The proportions of COGs functional categories of core genes, accessory genes, and unique genes. J, translation, ribosomal structure and biogenesis; K, transcription; L, replication, recombination, and repair; B, chromatin structure and dynamics; D, cell cycle control, cell division, and chromosome partitioning; V, defense mechanisms; T, signal transduction mechanisms; M, cell wall/membrane/envelope biogenesis; N, cell motility; Z, cytoskeleton; W, extracellular structures; U, intracellular trafficking, secretion, and vesicular transport; O, posttranslational modification, protein turnover, and chaperones; C, energy production and conversion; G, carbohydrate transport and metabolism; E, amino acid transport and metabolism; F, nucleotide transport and metabolism; H, coenzyme transport and metabolism; I, lipid transport and metabolism; P, inorganic ion transport and metabolism; Q, secondary metabolite biosynthesis, transport, and catabolism; R, general function prediction only; S, function unknown.

FIG 4

The genes and pathways related to carotenoid and bacteriochlorophyll a biosynthesis of bacteria within the genus Qipengyuania. (a) The arrangement of the carotenoid biosynthesis-related genes. (b) The NJ phylogenetic tree based on the hyc gene sequences and the heatmap of pairwise similarities. Bootstrap values greater than 50% are shown at branch points. Bar, 0.2 represents nucleotide substitutions per site. (c) Colony colors of two representative strains, YG19^T and GH1^T. (d) The UV-VIS absorption spectra of carotenoids of two representative strains, YG19^T and GH1^T. (e) The arrangement of the bacteriochlorophyll a biosynthesis-related genes. (f and g) The phylogenetic trees based on BchY and PufM sequences. The sequences of reference strains are selected by a concise Microbial Protein BLAST search. Accession numbers of individuals are denoted in parentheses. Bootstrap values greater than 50% are shown at branch points. Bar, 0.02/0.05 nucleotide substitution rate (Knuc) units.