Stability of toxin gene proportion in red-pigmented populations of the cyanobacterium Planktothrix during 29 years of re-oligotrophication of Lake Zürich

Abstract

BackgroundHarmful algal blooms deteriorate the services of aquatic ecosystems. They are often formed by cyanobacteria composed of genotypes able to produce a certain toxin, for example, the hepatotoxin microcystin (MC), but also of nontoxic genotypes that either carry mutations in the genes encoding toxin synthesis or that lost those genes during evolution. In general, cyanobacterial blooms are favored by eutrophication. Very little is known about the stability of the toxic/nontoxic genotype composition during trophic change.ResultsArchived samples of preserved phytoplankton on filters from aquatic ecosystems that underwent changes in the trophic state provide a so far unrealized possibility to analyze the response of toxic/nontoxic genotype composition to the environment. During a period of 29 years of re-oligotrophication of the deep, physically stratified Lake Zürich (1980 to 2008), the population of the stratifying cyanobacterium Planktothrix was at a minimum during the most eutrophic years (1980 to 1984), but increased and dominated the phytoplankton during the past two decades. Quantitative polymerase chain reaction revealed that during the whole observation period the proportion of the toxic genotype was strikingly stable, that is, close to 100%. Inactive MC genotypes carrying mutations within the MC synthesis genes never became abundant. Unexpectedly, a nontoxic genotype, which lost its MC genes during evolution, and which could be shown to be dominant under eutrophic conditions in shallow polymictic lakes, also co-occurred in Lake Zürich but was never abundant. As it is most likely that this nontoxic genotype contains relatively weak gas vesicles unable to withstand the high water pressure in deep lakes, it is concluded that regular deep mixing selectively reduced its abundance through the destruction of gas vesicles.ConclusionsThe stability in toxic genotype dominance gives evidence for the adaptation to deep mixing of a genotype that retained the MC gene cluster during evolution. Such a long-term dominance of a toxic genotype draws attention to the need to integrate phylogenetics into ecological research as well as ecosystem management.

Sedimentary DNA Reveals Cyanobacterial Community Diversity over 200 Years in Two Perialpine Lakes

“…The latter finding is consistent with early reports of the presence of P. rubescens (formerly Oscillatoria rubescens) forming large reddish blooms known as the Burgundy blood phenomenon at the surface of Lake Zurich in 1897 (61,62) and with a recent study showing that a single genotype of P. rubescens constituted almost 100% of the lake's population over almost 30 years (1980 to 2008) (63).…”

Predicting blooms of toxic cyanobacteria in eutrophic lakes with diverse cyanobacterial communities

“…The share of toxic genotypes in P . rubescens is stable during the vegetation season and is close to 100% 12 , 44 . This stability makes it possible to predict whether the cyanobacterial blooms, if they occur, will be toxic.…”

Phytoplankton functional composition shows higher seasonal variability in a large shallow lake after a eutrophic past

“…, Ostermaier et al. ), but their share is expected to eventually diminish in the future in case the oligotrophication process continues (Fastner et al. ), which is a probable scenario for the lake due to the significant reduction in nutrient loads (Istvánovics et al.…”

“…It is important to note that the maximum extent of annual variability would not necessarily have increased during the post-eutrophic era without the late summer dominance of cyanobacteria still remaining characteristic. The persistence of cyanobacterial dominance during reoligotrophication is not unusual (Jeppesen et al 2005, Ostermaier et al 2012), but their share is expected to eventually diminish in the future in case the oligotrophication process continues (Fastner et al 2016), which is a probable scenario for the lake due to the significant reduction in nutrient loads . From this, we can assume that the inflated probability space may depict a transitional period, and how the borders of annual variability will shift in the future is hard to tell.…”