Introduction
Phytoplankton play a vital role in lake ecosystems as primary producers at the base of aquatic food webs. Changes in their community composition in response to environmental change can have extensive ecological and biogeochemical implications (Litchman et al ., 2015). Many lakes worldwide are experiencing rapid rates of change in response to multiple interacting stressors, but our understanding of how phytoplankton communities respond is limited (Carpenter et al ., 2011; Heinoet al ., 2009). Multi-decadal records of phytoplankton communities can enable us to understand how they have responded to past environmental change and provide insight for how they may respond in the future (Willis et al ., 2010).
Detailed long-term monitoring of the phytoplankton community is restricted to a relatively small number of well-studied lakes (Burlakovaet al ., 2018; Hampton et al ., 2008). Where long-term monitoring records are not available, a range of proxies can be used to produce historical records of the phytoplankton community, such as microfossils and pigments extracted from lake sediment cores (Davidson and Jeppesen, 2013). Microfossil analysis is a widely used technique but is limited to organisms with well-preserved and morphologically distinct remains, such as diatom frustules (Hembrow et al ., 2014; Leira, 2005) and the resting cysts produced by some dinoflagellates (Drljepanet al ., 2014). Photosynthetic pigments can provide a record of eukaryotic algal and cyanobacterial community composition, abundance, and primary productivity (Griffiths et al ., 2022; Kpodonuet al ., 2016; Makri et al ., 2019; Watanabe et al ., 2012), but many pigments are not specific enough to enable taxonomic identification beyond the class level (Gong et al ., 2020). These limitations of traditional palaeolimnological techniques highlight the need for complementary and improved methods which can be applied to a wider diversity of organisms, such as sedimentary DNA (sedDNA).
sedDNA is a promising palaeolimnological approach which can be used to reconstruct past communities using DNA preserved within lake sediment cores (Edwards, 2020). DNA from living organisms is deposited in the lake sediment, where it is preserved and progressively buried over time. This DNA can then be extracted from layers of a sediment core and sequenced to produce a temporal record of lake communities (Capoet al ., 2021; Thorpe et al ., 2022). sedDNA offers many potential benefits compared to traditional palaeolimnological techniques. For example, a relatively high taxonomic resolution can be achieved, and high-throughput amplicon sequencing can process many hundreds or even thousands of samples relatively quickly (Bohmannet al ., 2022; Gong et al ., 2020; Mejbel et al ., 2021). A wider diversity of organisms can be studied using sedDNA, including those previously overlooked with microfossil analysis due to a lack of well-preserved and morphologically distinct remains (Domaizonet al ., 2017). The applicability of sedDNA to the wider community, including eukaryotic algae (Capo et al ., 2016), bacteria (Thorpe et al ., 2022), zooplankton (Tsugeki et al ., 2022) and macrophytes (Stoof-Leichsenring et al ., 2022) allows a more complete reconstruction of ecosystem structure which may, in turn, facilitate inferences on past trophic interactions (Barouilletet al ., 2022; Ellegaard et al ., 2020).
sedDNA is becoming more widely used in palaeolimnology, but there are currently some uncertainties surrounding the deposition and taphonomy of DNA in lakes (Capo et al ., 2021; 2022). The extent and rate of DNA degradation may vary among taxa and depend upon the state in which DNA is deposited. For example, intracellular DNA or DNA bound to mineral particles is typically better protected from degradation processes, such as oxidation, hydrolysis, and bacterial degradation than free extracellular DNA (Giguet-Covex et al ., 2019; Mauvisseau et al ., 2022). The depositional and degradational processes DNA is subject to could affect the ability of sedDNA to provide a reliable record of past phytoplankton communities. Although sedDNA has previously been found to be broadly comparable with records from diatom frustules (Anslan et al ., 2022) and photosynthetic pigments (Picardet al ., 2022; Tse et al ., 2018), these traditional palaeolimnological tools are also subject to pre- and post-depositional losses and subsequent biases. Validation of sedDNA against long-term monitoring of phytoplankton in the water column is therefore needed to further the development of sedDNA as a reliable and robust record of past microbial communities.
To address this need, we analyse and compare sedDNA and water column phytoplankton data from Esthwaite Water, a relatively small lake in the English Lake District which has experienced well-documented changes in human activity and has undergone substantial eutrophication in recent decades (Dong et al ., 2011; Maberly et al ., 2011). Lake physicochemical conditions and the phytoplankton community have been continually monitored since 1945, providing a detailed record against which palaeolimnological records can be compared and validated. Esthwaite Water has been the site of several studies investigating seasonal trends in phytoplankton communities in the water column (Feuchtmayr et al ., 2012; Talling and Heaney, 2015), and palaeolimnological studies of the bacterial and cyanobacterial community as measured by sedDNA (Thorpe et al ., 2022), and the microbial eukaryotic community as measured with photosynthetic pigments (Moorhouseet al ., 2017) and diatom frustules (Bennion et al ., 2000; Dong et al ., 2011, 2012). Our study, which combines concurrent microscopy-based monitoring and sedDNA records, is therefore uniquely placed to determine whether sedDNA is a reliable tool for reconstruction of past trends in phytoplankton community composition.