The Trait Repertoire Enabling Cyanobacteria to Bloom Assessed through Comparative Genomic Complexity and Metatranscriptomics

Abstract

Water bloom development due to eutrophication constitutes a case of niche specialization among planktonic cyanobacteria, but the genomic repertoire allowing bloom formation in only some species has not been fully characterized. We posited that the habitat relevance of a trait begets its underlying genomic complexity, so that traits within the repertoire would be differentially more complex in species successfully thriving in that habitat than in close species that cannot. To test this for the case of bloom-forming cyanobacteria, we curated 17 potentially relevant query metabolic pathways and five core pathways selected according to existing ecophysiological literature. The available 113 genomes were split into those of blooming (45) or nonblooming (68) strains, and an index of genomic complexity for each strain’s version of each pathway was derived. We show that strain versions of all query pathways were significantly more complex in bloomers, with complexity in fact correlating positively with strain blooming incidence in 14 of those pathways. Five core pathways, relevant everywhere, showed no differential complexity or correlations. Gas vesicle, toxin and fatty acid synthesis, amino acid uptake, and C, N, and S acquisition systems were most strikingly relevant in the blooming repertoire. Further, we validated our findings using metagenomic gene expression analyses of blooming and nonblooming cyanobacteria in natural settings, where pathways in the repertoire were differentially overexpressed according to their relative complexity in bloomers, but not in nonbloomers. We expect that this approach may find applications to other habitats and organismal groups. IMPORTANCE We pragmatically delineate the trait repertoire that enables organismal niche specialization. We based our approach on the tenet, derived from evolutionary and complex-system considerations, that genomic units that can significantly contribute to fitness in a certain habitat will be comparatively more complex in organisms specialized to that habitat than their genomic homologs found in organisms from other habitats. We tested this in cyanobacteria forming harmful water blooms, for which decades-long efforts in ecological physiology and genomics exist. Our results essentially confirm that genomics and ecology can be linked through comparative complexity analyses, providing a tool that should be of general applicability for any group of organisms and any habitat, and enabling the posing of grounded hypotheses regarding the ecogenomic basis for diversification.

The special and general mechanism of cyanobacterial harmful algal blooms

“…Gas vesicles are well-known for their roles in buoyancy regulation, allowing cyanobacteria to position themselves in the water column for optimal resource utilization (Carey et al, 2012;Walsby et al, 1997). This pathway is more enriched in blooming than non-blooming species and correlated with the blooming incidence of cyanobacteria recorded in the literature (Cao et al, 2020): nearly all blooming species have at least one copy of the gvpA and gvpC genes, and the genes gvpFGJKNVWX, while all but one non-blooming species do not have any of these genes (Figure 7A). This pathway operates independently of other pathways, without a direct association with central metabolism.…”

“…Elevated nutrients in eutrophic waters-macro or trace, persistent or pulse-are the drivers of CyanoHABs (Heisler et al, 2008). The relevant biological functions assimilating and converting them into biomass, as synthetic media converted into cells in lab cultures, have been recently identified by comparative genomics between blooming and non-blooming species (Cao et al, 2020). They are also made available as a database, CyanoPATH (Du et al, 2020) (Figure 6).…”

“…The synthetases are nonribosomal peptide synthetase (ava-3855), ATP-grasp family enzyme (ava-3856), O-methyltransferase (ava_3857), and a dehydroquinate synthase (ava_3858). Interestingly, only some of the blooming species have one cluster whereas non-blooming species do not contain any (Cao et al, 2020). Considering the multiple factors in the mechanism, further empirical tests and theoretic are needed to make a better synthesis of the mechanism.…”

“…CCM is the step concentrating CO2 in carboxysomes to high levels (~ 40µM) for effective incorporation into ribulose bisphosphate in the Calvin cycle. CCM is more enriched in blooming than non-blooming species (Cao et al, 2020(Cao et al, ) et al, 2020. The CCM genes encode four types of functions: ccmKLMNO (structural proteins forming the carboxysome), icfA (carbonic anhydrase), bicA and sbtA (bicarbonate facilitator), cdnF3D3chY, cdnF4D4chX, and cmpABCD (ABC transporter for HCO3 -), and rbcLS (ribulose bisphosphate carboxylase/oxygenase).…”

Genetic, Genomics, and Responses to Stresses in Cyanobacteria: Biotechnological Implications

“…Currently, about 2000 complete or draft sequences of cyanobacterial genomes are accessible in public data bases such as the DOE joint genome institute (https://genome.jgi.doe.gov/portal/, accessed on 15 March 2021) and the Microbial Genome Database for Comparative Analysis (http: //mbgd.genome.ad.jp/, accessed on 15 March 2021). This number is steadily increasing in the frame of metagenomic analyses [49][50][51][52].…”