Dataset Information

Phylogenetic and evolutionary patterns in microbial carotenoid biosynthesis are revealed by comparative genomics.

ABSTRACT:

Background

Carotenoids are multifunctional, taxonomically widespread and biotechnologically important pigments. Their biosynthesis serves as a model system for understanding the evolution of secondary metabolism. Microbial carotenoid diversity and evolution has hitherto been analyzed primarily from structural and biosynthetic perspectives, with the few phylogenetic analyses of microbial carotenoid biosynthetic proteins using either used limited datasets or lacking methodological rigor. Given the recent accumulation of microbial genome sequences, a reappraisal of microbial carotenoid biosynthetic diversity and evolution from the perspective of comparative genomics is warranted to validate and complement models of microbial carotenoid diversity and evolution based upon structural and biosynthetic data.

Methodology/principal findings

Comparative genomics were used to identify and analyze in silico microbial carotenoid biosynthetic pathways. Four major phylogenetic lineages of carotenoid biosynthesis are suggested composed of: (i) Proteobacteria; (ii) Firmicutes; (iii) Chlorobi, Cyanobacteria and photosynthetic eukaryotes; and (iv) Archaea, Bacteroidetes and two separate sub-lineages of Actinobacteria. Using this phylogenetic framework, specific evolutionary mechanisms are proposed for carotenoid desaturase CrtI-family enzymes and carotenoid cyclases. Several phylogenetic lineage-specific evolutionary mechanisms are also suggested, including: (i) horizontal gene transfer; (ii) gene acquisition followed by differential gene loss; (iii) co-evolution with other biochemical structures such as proteorhodopsins; and (iv) positive selection.

Conclusions/significance

Comparative genomics analyses of microbial carotenoid biosynthetic proteins indicate a much greater taxonomic diversity then that identified based on structural and biosynthetic data, and divides microbial carotenoid biosynthesis into several, well-supported phylogenetic lineages not evident previously. This phylogenetic framework is applicable to understanding the evolution of specific carotenoid biosynthetic proteins or the unique characteristics of carotenoid biosynthetic evolution in a specific phylogenetic lineage. Together, these analyses suggest a "bramble" model for microbial carotenoid biosynthesis whereby later biosynthetic steps exhibit greater evolutionary plasticity and reticulation compared to those closer to the biosynthetic "root". Structural diversification may be constrained ("trimmed") where selection is strong, but less so where selection is weaker. These analyses also highlight likely productive avenues for future research and bioprospecting by identifying both gaps in current knowledge and taxa which may particularly facilitate carotenoid diversification.

SUBMITTER: Klassen JL

PROVIDER: S-EPMC2889829 | biostudies-literature |

REPOSITORIES: biostudies-literature

ACCESS DATA

Similar Datasets

Project description:Genome mining tools have enabled us to predict biosynthetic gene clusters that might encode compounds with valuable functions for industrial and medical applications. With the continuously increasing number of genomes sequenced, we are confronted with an overwhelming number of predicted clusters. In order to guide the effective prioritization of biosynthetic gene clusters towards finding the most promising compounds, knowledge about diversity, phylogenetic relationships and distribution patterns of biosynthetic gene clusters is necessary.Here, we provide a comprehensive analysis of the model actinobacterial genus Amycolatopsis and its potential for the production of secondary metabolites. A phylogenetic characterization, together with a pan-genome analysis showed that within this highly diverse genus, four major lineages could be distinguished which differed in their potential to produce secondary metabolites. Furthermore, we were able to distinguish gene cluster families whose distribution correlated with phylogeny, indicating that vertical gene transfer plays a major role in the evolution of secondary metabolite gene clusters. Still, the vast majority of the diverse biosynthetic gene clusters were derived from clusters unique to the genus, and also unique in comparison to a database of known compounds. Our study on the locations of biosynthetic gene clusters in the genomes of Amycolatopsis' strains showed that clusters acquired by horizontal gene transfer tend to be incorporated into non-conserved regions of the genome thereby allowing us to distinguish core and hypervariable regions in Amycolatopsis genomes.Using a comparative genomics approach, it was possible to determine the potential of the genus Amycolatopsis to produce a huge diversity of secondary metabolites. Furthermore, the analysis demonstrates that horizontal and vertical gene transfer play an important role in the acquisition and maintenance of valuable secondary metabolites. Our results cast light on the interconnections between secondary metabolite gene clusters and provide a way to prioritize biosynthetic pathways in the search and discovery of novel compounds.

Project description:To understand the evolution of coscinodiscophycean diatoms, plastome sequences of six coscinodiscophycean diatom species were constructed and analyzed in this study, doubling the number of constructed plastome sequences in Coscinodiscophyceae (radial centrics). The platome sizes varied substantially in Coscinodiscophyceae, ranging from 119.1 kb of Actinocyclus subtilis to 135.8 kb of Stephanopyxis turris. Plastomes in Paraliales and Stephanopyxales tended to be larger than those in Rhizosoleniales and Coscinodiacales, which were due to the expansion of the inverted repeats (IRs) and to the marked increase of the large single copy (LSC). Phylogenomic analysis indicated that Paralia and Stephanopyxis clustered tightly to form the Paraliales-Stephanopyxales complex, which was sister to the Rhizosoleniales-Coscinodiscales complex. The divergence time between Paraliales and Stephanopyxales was estimated at 85 MYA in the middle Upper Cretaceous, indicating that Paraliales and Stephanopyxales appeared later than Coscinodiacales and Rhizosoleniales according to their phylogenetic relationships. Frequent losses of housekeeping protein-coding genes (PCGs) were observed in these coscinodiscophycean plastomes, indicating that diatom plastomes showed an ongoing reduction in gene content during evolution. Two acpP genes (acpP1 and acpP2) detected in diatom plastomes were found to be originated from an early gene duplication event occurred in the common progenitor after diatom emergence, rather than multiple independent gene duplications occurring in different lineages of diatoms. The IRs in Stephanopyxis turris and Rhizosolenia fallax-imbricata exhibited a similar trend of large expansion to the small single copy (SSC) and slightly small contraction from the LSC, which eventually led to the conspicuous increase in IR size. Gene order was highly conserved in Coscinodiacales, while multiple rearrangements were observed in Rhizosoleniales and between Paraliales and Stephanopyxales. Our results greatly expanded the phylogenetic breadth in Coscinodiscophyceae and gained novel insights into the evolution of plastomes in diatoms.