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.