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.

Figure 1

Location of the 12 lakes across the globe. These samples represent a 280° longitudinal and 90° latitudinal gradient.

Figure 2

(a) Relative abundance of Bacteria classes or subclasses in the nine lakes. The lakes are arranged in order from left to right of increasing percent Microcystis in the community. Classes less than 1% of the total relative abundance were grouped together as a single group denoted “<1% abund.” Oxyphotobacteria (cyanobacteria) were split into two groups: Microcystis only in one and all other cyanobacteria in the second. (b) Relative abundance of non‐Microcystis (i.e., microbiome) bacterial classes.

Figure 3

Scatter plots of community dissimilarity in the microbiome as related to geographic distance. (a) The nonsignificant (GLM deviance explained = 3.7%, p = 0.2) relationship between taxonomic Bray–Curtis dissimilarity and geographic distance where the higher Bray–Curtis values indicate fewer species in common between sites. (b) Abundance weighted UniFrac did not scale significantly by geographic distance (GLM DE = 0.82%, p = 0.55). Here, higher values of UniFrac indicate there is little overlap in species between communities whereas lower values indicate the communities are more similar.

Figure 4

Distributions of within community phylogenetic relatedness (αNTI, nearest taxon index), and the phylogenetic relatedness between two communities (βNTI) of the nine sampled lakes. Values below −2 or above +2 SD from the null (indicated by the red rectangle) are statistically significantly different from random. Black dashed lines indicate the mean of the observed distributions. The mean of the αNTI distribution is 4.64 and the mean of the βNTI distribution is −3.58. αNTI is a measure of community phylogenetic structure and relatedness, where positive deviations from the null expectation indicate the species in the community are more phylogenetically related (clustered) than expected by chance (as seen here), and negative deviations indicate the species are more phylogenetically distant (overdispersed). The observed αNTI was significantly different from the null (t = 10.13, p < 0.001). βNTI measures phylogenetic relatedness between two communities with values greater than the null meaning lower relatedness than expected by chance and values lower than the null meaning higher relatedness than expected by chance (as seen here). Our βNTI is significantly different from random (t = −12.65, p < 0.001).

Figure 5

The dissimilarity between the Microcystis microbiome community's metagenomic function was not significantly correlated with geographic distance (GLM DE = 1.97%, p = 0.41) and was overall low (low values of Bray–Curtis dissimilarity).

Figure 6

Venn diagram showing the distribution of complete or nearly complete (no more than one gene missing) KEGG modules in Microcystis and the microbiome bacteria. See Supplementary Table S2 for details and indication for involvement in major elemental cycling. KEGG modules in bold print with asterisks were detected in the full metagenome data but not in the Microcystis or the microbiome bacterial MAGs.