Effects of nutrients and warming on Planktothrix dynamics and diversity: a palaeolimnological view based on sedimentary DNA and RNA

Abstract

1. Decennial changes in Planktothrix rubescens diversity and dynamics were reconstructed by applying molecular tools to analyse DNA and RNA extracted from lake sediments. The sediments studied were sampled from a deep peri-alpine lake that has experienced both dramatic shifts in trophic conditions and large-scale climatic changes. Palaeolimnological proxies were combined with statistical modelling to investigate the relative influence of phosphorus concentrations and temperature changes on the extent of Planktothrix blooms over the last century. 2. Phylogenetic analysis revealed that the overall composition of the cyanobacterial community changed over the transition from oligotrophic to eutrophic conditions. When the relative abundance of Planktothrix decreased in the 1970s, concomitant with eutrophication, total cyanobacterial abundance remained high and more Anabaena and Microcystis sequences were detected. In spite of such drastic environmental changes, the lake provided a constant niche for one particular Planktothrix species, which was consistently present from the 1920s to the present day. 3. Phosphorus concentration was found to be the dominant driver of the relative abundance of P. rubescens, with the highest abundances observed during mesotrophic conditions. The relative role of climate was nutrient-dependent, with warmer springs having a positive effect on P. rubescens abundance only during mesotrophic periods. 4. Overall, this study confirms that analysis of genetic signatures preserved in sediment archives allows assessment of key palaeoenvironmental indicator species that have no diagnostic microscopic cellular features in the sediment record. In the case of cyanobacteria, palaeogenetics offer unique opportunities to anticipate how future climate change might affect the response of P. rubescens to phosphorus concentration.

High-resolution paleolimnology opens new management perspectives for lakes adaptation to climate warming

“…Finally, the respective contribution of climate change vs. local forcings in driving observed ecological changes, such as the time-period at which they contributed to these changes, could be hierarchized, based on Generalized additive models (GAM, Simpson and Anderson, 2009). (Savichtcheva et al, 2011(Savichtcheva et al, , 2014 Bourget (2000)(2001)(2002)(2003)(2004)(2005)(2006)(2007)(2008)(2009)(2010) Geneva (1977-) Annecy (1992-) Pico-cyanobacteria abundances and taxonomic composition Q-PCR Sequencing* on 16SrRNA gene +ITS (Domaizon et al, 2013) Littoral and benthic chironomids Spatially structured chironomid assemblages (Frossard et al, , 2014 Daphnia gene flow Micro-satelitte analyses of Daphnia resting eggs (Alric, 2012) Geochemistry Carbon cycling δ 13 C of sub-fossil remains (Perga, 2010(Perga, , 2011Frossard et al, 2014Frossard et al, , 2015 Hypoxic volumes 3D Distribution of laminated sediments (Jenny et al, , 2014a Lakes Geneva, Bourget, and Annecy are young lakes originating from the last deglaciation, located on the northwest edge of the French Alps (Figure 1). They belong to a similar hydro-ecoregion.…”

“…Past abundances of cyanobacteria, including picocyanobacteria (qPCR), and changes in their phylogenetic compositions [sequencing of the 16S rRNA and internally transcribed spacer region (Domaizon et al, 2013;Savichtcheva et al, 2014)] were reconstructed over 150 years and the role of climate warming as compared to lake trophic status on the quantitative and qualitative changes was quantified. As for diatoms, changes in TP was the dominant driver of cyanobacteria species successions, even at the scale of picocyanobacterial phylogenetic transitions, while air temperatures had a significant influence on both the colonial/filamentous cyanobacterial and picocyanobacterial abundances (Domaizon et al, 2013;Savichtcheva et al, 2014). Hence, blooming episodes of the toxic P. rubescens in Lake Bourget occurred at oligomesotrophic state (i.e., in the 1970s and in the 1990s) but warmer waters in the last quarter of the XXth century amplified their abundances as compared to the 1970s.…”

“…Hence, blooming episodes of the toxic P. rubescens in Lake Bourget occurred at oligomesotrophic state (i.e., in the 1970s and in the 1990s) but warmer waters in the last quarter of the XXth century amplified their abundances as compared to the 1970s. Current re-oligotrophication Lake Bourget has recently operated a transition from Planktothrix dominance to Anabaena and Microcystis within colonial/filamentous cyanobacterial communities which abundances are yet maintained high by still warming climate (Savichtcheva et al, 2014). Therefore, the consequences of climate warming at all cyanobacterial levels have been conditioned by TP levels in the lakes (Figure 4B).…”

“…Most of the experimental works so far have focused on changes in total growth rates or total biomass, suggesting that under warmer waters, nutrient use efficiency might be higher (De Senerpont Domis et al, 2013). Longterm cyanobacterial and pico-cyanobacterial transitions in Lake Bourget support these outputs suggesting that temperaturedependent stoichiometric constrains might also control species transitions under warmer climate (Domaizon et al, 2013;Savichtcheva et al, 2014).…”

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

“…Recent sedaDNA-based studies were applied to investigate diversity changes in phytoplankton (18) and cyanobacterial communities (19) during the Holocene. The abundance and diversity of natural populations of cyanobacteria have been investigated in sedimentary archives of perialpine lakes using quantitative PCR and cloning (20)(21)(22). Sedimentary DNA has also been used to investigate the past distribution and diversity of potentially toxic Microcystis in Lake Erie (23) and the saxitoxin-producing Cylindrospermopsis raciborskii in a subtropical lagoon (24).…”