Ecogenomics and Taxonomy of Cyanobacteria Phylum

Abstract

Cyanobacteria are major contributors to global biogeochemical cycles. The genetic diversity among Cyanobacteria enables them to thrive across many habitats, although only a few studies have analyzed the association of phylogenomic clades to specific environmental niches. In this study, we adopted an ecogenomics strategy with the aim to delineate ecological niche preferences of Cyanobacteria and integrate them to the genomic taxonomy of these bacteria. First, an appropriate phylogenomic framework was established using a set of genomic taxonomy signatures (including a tree based on conserved gene sequences, genome-to-genome distance, and average amino acid identity) to analyse ninety-nine publicly available cyanobacterial genomes. Next, the relative abundances of these genomes were determined throughout diverse global marine and freshwater ecosystems, using metagenomic data sets. The whole-genome-based taxonomy of the ninety-nine genomes allowed us to identify 57 (of which 28 are new genera) and 87 (of which 32 are new species) different cyanobacterial genera and species, respectively. The ecogenomic analysis allowed the distinction of three major ecological groups of Cyanobacteria (named as i. Low Temperature; ii. Low Temperature Copiotroph; and iii. High Temperature Oligotroph) that were coherently linked to the genomic taxonomy. This work establishes a new taxonomic framework for Cyanobacteria in the light of genomic taxonomy and ecogenomic approaches.

Keywords: charting biodiversity; ecological niches; genome-based microbial taxonomy; high-throughput sequencing technology; metagenome; microbial ecology.

Figure 1

Phylogenomic tree of the Cyanobacteria phylum with the proposed new names. Tree construction was performed using 100 genomes (ninety-nine used in this study plus the outgroup), based on a set of conserved marker genes. The numbers at the nodes indicate bootstrap values as percentages greater than 50%. Bootstrap tests were conducted with 1,000 replicates. The unit of measure for the scale bars is the number of nucleotide substitutions per site. The Gloeobacter violaceus PCC 7421 sequence was designated as outgroup. Capital letters indicate environmental source: F, freshwater; M, marine; P, peat bog (sphagnum); S, soil; T, thermal; and §, other habitat. New names are highlighted in red. Overwritten T indicates type strain or type species. Ecogenomic groups are depicted in different colors as indicated in the legend: Low Temperature group; Low Temperature Copiotroph group; and High Temperature Oligotroph group. Cases depicted in the Results section are in bold.

Figure 2

Heatmap displaying the AAI levels between cyanobacterial genomes. The intraspecies limit is assumed as ≥95%, whereas genera delimitation is assumed as ≥70% (dashed lines) AAI. Clustering the genomes by AAI similarity was done using a hierarchical clustering method in R (hclust), based on Manhattan distances. The AAI values are associated with the respective thermal color scale located at the bottom left corner of the figure. The proposed new genera and species names were adopted in this figure.

Figure 3

Correlations between Cyanobacteria and environmental variables. Heatmap displays Spearman correlation scores between the abundance of cyanobacterial genomes and measured environmental parameters at Tara Ocean sampling sites. Correlations that showed q corrected p < 0.05 are marked with stars. Variables were grouped through the complete linkage clustering method using Manhattan distances as input. The proposed new genera and species names were adopted in this figure.

Figure 4

Ecogenomic analysis of Cyanobacteria in global marine environments. (A) Distribution of the dominant ecogenomic groups (Low Temperature group; Low Temperature Copiotroph group; and High Temperature Oligotroph) along the Tara Ocean transect sampling from surface layer (5 m). (B) Distribution of the dominant ecogenomic groups along the Tara Ocean transect sampling from subsurface layer (>5 m). (C) Non-metric multidimensional scaling (NMDS) analysis of the marine metagenomes and environmental parameters. Ordination plot of physicochemical parameters. Dots indicate the metagenomes samples. Distances were calculated based on the Bray-Curtis Method. NMDS stress value = 0.15. (D) Non-metric multidimensional scaling (NMDS) analysis of the marine metagenomes and environmental parameters. Ordination plot of ecogenomic clusters. Dots indicate the metagenomes samples. Distances were calculated based on the Bray-Curtis Method. NMDS stress value = 0.15.