Benthic Archives Reveal Recurrence and Dominance of Toxigenic Cyanobacteria in a Eutrophic Lake over the Last 220 Years

Abstract

Akinetes are resistant cells which have the ability to persist in sediment for several decades. We have investigated the temporal distribution of akinetes of two species, Dolichospermum macrosporum and Dolichospermum flos-aquae, in a sediment core sampled in Lake Aydat (France), which covers 220 years. The upper part, from 1907 to 2016, the number of akinetes fluctuated but stayed at high concentrations, especially for D. macrosporum in surface sediment (with the maximal value close to 6.105 akinetes g DW−1 of sediment), suggesting a recurrence of blooms of this species which was probably closely related to anthropic eutrophication since the 1960s. Before 1907, the abundance of akinetes of both species was very low, suggesting only a modest presence of these cyanobacteria. In addition, the percentage of intact akinetes was different for each species, suggesting different ecological processes in the water column. This percentage also decreased with depth, revealing a reduction in germination potential over time. In addition, biosynthetic genes of anatoxin-a (anaC) and microcystin (mcyA) were detected. First results show a high occurrence of mcyA all down the core. In contrast, anaC gene was mostly detected in the surface sediment (since the 1980s), revealing a potentially more recent occurrence of this cyanotoxin in Lake Aydat which may be associated with the recurrence of blooms of D. macrosporum and thus with anthropic activities.

Is a Central Sediment Sample Sufficient? Exploring Spatial and Temporal Microbial Diversity in a Small Lake

“…Together with the rising usage of fertilizers, this has caused significant nutrient enrichments in the region's waterways [43]. An increase of cyanobacteria during the 1900s was also observed in other lake sediment studies of North America [4] and Europe [6] and was linked to nutrient enrichment as a result of intensified agriculture.…”

“…MCs are synthesized non-ribosomally by a large multifunctional enzyme complex which contains both non-ribosomal peptide synthetase and polyketide synthase domains [13]. The mcy gene cluster (mcyA-J) encoding these biosynthetic enzymes has been employed as the target region for the molecular detection of potentially toxin producing cyanobacteria strains in water and sediment [6,14,15].…”

“…Both cyanobacterial DNA and MCs are thought to be well preserved in sediments, and both have been detected in sediment layers dating back over 200 years [6][7][8][9][10]. Most paleolimnological studies on cyanobacteria [6] but also eukaryotes [23,24], collect sediment cores from a single central site or deepest point in a lake, assuming a relatively even distribution across the lake. However, during a bloom cell densities of buoyant cyanobacteria, e.g., Microcystis spp., are highly dependent on wind and current drift, hence there is often high spatial variability across a lake surface [25][26][27].…”

“…Contact with or ingestion of water contaminated with cyanotoxins can lead to poisoning, or death of humans, pets, stock, and wildlife [ 5 ]. Amongst the cyanobacterial toxins, the cyclic heptapeptide microcystins (MCs) are the most frequently found [ 6 , 7 , 8 , 9 , 10 ].…”

“…An emerging technique that can contribute historic data is the application of molecular biological methods to sediment core analysis [ 19 ]. Employing molecular techniques, e.g., metabarcoding and droplet digital PCR (ddPCR), allows reconstruction of historical cyanobacteria communities using phylogenetic marker genes like the 16S ribosomal RNA (16S rRNA) but also functional genes (such as the mcy gene cluster) identified in sediment samples [ 6 , 7 ]. Accumulation of cyanobacterial DNA and toxins in sediments occurs via natural cell sedimentation during and after blooms [ 20 ].…”