Spatio-temporal connectivity of the aquatic microbiome associated with cyanobacterial blooms along a Great Lake riverine-lacustrine continuum

Abstract

Lake Erie is subject to recurring events of cyanobacterial harmful algal blooms (cHABs), but measures of nutrients and total phytoplankton biomass seem to be poor predictors of cHABs when taken individually. A more integrated approach at the watershed scale may improve our understanding of the conditions that lead to bloom formation, such as assessing the physico-chemical and biological factors that influence the lake microbial community, as well as identifying the linkages between Lake Erie and the surrounding watershed. Within the scope of the Government of Canada's Genomics Research and Development Initiative (GRDI) Ecobiomics project, we used high-throughput sequencing of the 16S rRNA gene to characterize the spatio-temporal variability of the aquatic microbiome in the Thames River-Lake St. Clair-Detroit River-Lake Erie aquatic corridor. We found that the aquatic microbiome was structured along the flow path and influenced mainly by higher nutrient concentrations in the Thames River, and higher temperature and pH downstream in Lake St. Clair and Lake Erie. The same dominant bacterial phyla were detected along the water continuum, changing only in relative abundance. At finer taxonomical level, however, there was a clear shift in the cyanobacterial community, with Planktothrix dominating in the Thames River and Microcystis and Synechococcus in Lake St. Clair and Lake Erie. Mantel correlations highlighted the importance of geographic distance in shaping the microbial community structure. The fact that a high proportion of microbial sequences found in the Western Basin of Lake Erie were also identified in the Thames River, indicated a high degree of connectivity and dispersal within the system, where mass effect induced by passive transport play an important role in microbial community assembly. Nevertheless, some cyanobacterial amplicon sequence variants (ASVs) related to Microcystis, representing less than 0.1% of relative abundance in the upstream Thames River, became dominant in Lake St. Clair and Erie, suggesting selection of those ASVs based on the lake conditions. Their extremely low relative abundances in the Thames suggest additional sources are likely to contribute to the rapid development of summer and fall blooms in the Western Basin of Lake Erie. Collectively, these results, which can be applied to other watersheds, improve our understanding of the factors influencing aquatic microbial community assembly and provide new perspectives on how to better understand the occurrence of cHABs in Lake Erie and elsewhere.

Keywords: Lake Erie watershed; aquatic microbiome; cyanobacteria; genetic connectivity; harmful algal blooms.

Figure 1

Location of the sampling sites colored by systems (Upper and Lower Thames Rivers, Lake St. Clair, Detroit River and Lake Erie). Map created with R using the open-access databases “worldHires” (https://www.evl.uic.edu/pape/data/WDB/) and river line downloaded from the Government of Canada Open Data Portal (http://open.canada.ca/en/open-data) and the National Weather service (https://www.weather.gov/gis/Rivers). Estimates of mean daily discharge from 2016 to 2019 were calculated from data available from the Water Survey of Canada (https://wateroffice.ec.gc.ca/) for the Thames River and from the U.S. National Water Information System (https://waterdata.usgs.gov/nwis) for the Maumee and Sandusky Rivers. Estimates of mean TP loads from 2016 to 2019 were calculated from the data available from ErieStat (https://www.blueaccounting.org/).

Figure 2

Non-metric multidimensional scaling (NMDS) of the microbial community based on Bray-Curtis distance, colored as a function of the system sampled overlaid with the significantly correlated environmental variables (A) and colored as a function of the season (B). WB stands for Western Basin and C&EB for Central and Eastern Basin, respectively.

Figure 3

Relative abundances of the main microbial phyla expressed as % of the microbial community (A) and cyanobacterial genera expressed as % of the cyanobacterial community (B) along the water continuum and as a function of the different seasons. The Western Basin (WB) is separated by a dotted line from CB for the Central Basin (CB) and Eastern Basin (EB). Not all systems were sampled during winter (for sampling frequency see Supplementary Table 1).

Figure 4

Intersection of ASVs across systems and seasons. Horizontal bars indicate the total number of ASVs for each system at each season and vertical bars represent the number of ASVs in the category designated by the dot below. Detroit River samples were lumped with Lake St. Clair samples and winter samples were removed due to lack of system represented. Only intersections of more than 100 ASVs are shown.

Figure 5

Proportion microbial reads (A) and ASVs (B), as well as Cyanobacterial reads (C) and ASVs (D) in the Lake Erie Western basin at different season, classified as a function of the most upstream system they were first detected in (WB stands for Western Basin). Winter samples were removed due to lack of system represented.

Figure 6

Neighbor-joining bootstrapped phylogenetic tree of the 15 most abundant cyanobacterial ASVs with sequences from culture representative of the BOLD reference database and sequences downloaded from GenBank with only bootstrap values above 50% from the 1,000 replicated trees indicated at the nodes of branches (A). Corresponding relative abundance in % of the microbial community of the single ASVs along the water continuum and across season colored based on their genera (B). WB stands for Western Basin.