The global Microcystis interactome

Abstract

Bacteria play key roles in the function and diversity of aquatic systems, but aside from study of specific bloom systems, little is known about the diversity or biogeography of bacteria associated with harmful cyanobacterial blooms (cyanoHABs). CyanoHAB species are known to shape bacterial community composition and to rely on functions provided by the associated bacteria, leading to the hypothesized cyanoHAB interactome, a coevolved community of synergistic and interacting bacteria species, each necessary for the success of the others. Here, we surveyed the microbiome associated with Microcystis aeruginosa during blooms in 12 lakes spanning four continents as an initial test of the hypothesized Microcystis interactome. We predicted that microbiome composition and functional potential would be similar across blooms globally. Our results, as revealed by 16S rRNA sequence similarity, indicate that M. aeruginosa is cosmopolitan in lakes across a 280 longitudinal and 90 latitudinal gradient. The microbiome communities were represented by a wide range of operational taxonomic units and relative abundances. Highly abundant taxa were more related and shared across most sites and did not vary with geographic distance, thus, like Microcystis, revealing no evidence for dispersal limitation. High phylogenetic relatedness, both within and across lakes, indicates that microbiome bacteria with similar functional potential were associated with all blooms. While Microcystis and the microbiome bacteria shared many genes, whole-community metagenomic analysis revealed a suite of biochemical pathways that could be considered complementary. Our results demonstrate a high degree of similarity across global Microcystis blooms, thereby providing initial support for the hypothesized Microcystis interactome.

Single-colony sequencing reveals phylosymbiosis, co-phylogeny, and horizontal gene transfer between the cyanobacterium Microcystis and its microbiome

“…Other AB ( e.g. , Roseomona s, Rhodobacter and Methylobacterium ) encoded genes involved in the anoxygenic photosynthesis (Supplementary Table 9) and genes related with the transport of rhamnose, D-xylose, fructose, glycerol and a-glucoside, which could also complement the metabolic repertoire of Microcystis 16 , although this deserves further study.…”

“…Phylosymbiosis and co-speciation appear to be relatively common and strong in mammalian gut microbiomes 22,23 , and even in the more environmentally-exposed coral microbiome 22,23 . and studies suggest that it may rely on nitrogen-fixing members of its microbiota 16,39 . While it remains unclear if metabolites are actually exchanged between Microcystis and members of its microbiome, these hypotheses could be tested experimentally.…”

“…The enclosed nature of animal guts reduces dispersal of microbiomes and favours vertical transmission, potentially leading to co-phylogeny without the need to invoke co-evolution 27 . In contrast, metagenomic sequencing suggests Microcystis and its microbiome are globally distributed 16 , making it unlikely that phylosymbiosis could arise due to common biogeography of Microcystis and its microbiome. On the other hand, Microcystis may be geographically structured on shorter evolutionary time scales, due to local adaptation or clonal expansions, and Microcystis genotypes might have distinct phenotypic characteristics that could select for distinct microbiomes 28,29 .…”

“…The Microcystis colony microbiome is distinct from the surrounding lake bacterial community, enriched in Proteobacteria and depleted in Actinobacteria 13,14 . The microbiome composition has been associated with temperature, seasonality, biogeography, Microcystis morphology and density 13,[15][16][17] . Lab experiments show the potential for AB to influence Microcystis growth and colony formation [18][19][20][21] .…”

“…Previous studies of the Microcystis microbiome have used either culture-independent metagenomics from lakes, a bulk biomass collection method which cannot resolve fine-scale spatial interaction within colonies ( e.g. , 16 ), or culture-based studies of Microcystis isolates, which have found host-microbiome divergence according to phosphorous gradients and taxonomy 30 , but may not be representative of the natural diversity of Microcystis or AB as they occur in nature. To combine the strengths of both these approaches, we developed a simple method for isolating individual Microcystis colonies directly from lakes, followed by DNA extraction and sequencing without a culture step 29 .…”