Temporal trends in community composition
In both records, chlorophytes, dinoflagellates, ochrophytes and
bacillariophytes displayed general increasing trends beginning around
1970-1990. These could be responses to nutrient enrichment, which
accelerated in Esthwaite Water from the 1970s and remained high until
the early 2000s (Supplementary Information, Fig. S2). A sediment core
has previously been collected from Esthwaite Water for sedimentary
pigment analysis. In this record, many algal pigments also displayed
increasing trends over time from the 1800s to 2011 with their highest
concentrations detected after the 1970s, including Chlorophyll band lutein, which are indicative of chlorophytes, and diatoxanthin,
which is indicative of bacillariophytes. However, there was a large peak
in the concentration of diatoxanthin around the 2000s, and this was not
reflected in the sedDNA or microscopy records for bacillariophytes
(Moorhouse et al ., 2018).
Co-occurring patterns in the microscopy record could support sedDNA as a
reliable record of past community change. The relative abundance and
occurrence of chlorophytes in the sedDNA and microscopy records,
respectively, both increased sharply in more recent samples. However,
the increase in chlorophyte relative abundance in the sedDNA record
occurred over a decade later than the increase in occurrence in the
microscopy record. Distinct peaks in the relative abundance and
occurrence of dinoflagellates were observed in the sedDNA and microscopy
records, but the timing of these peaks was also not aligned. sedDNA and
microscopy may have recorded the same trends, but they may have been
off-set due to uncertainties in the chronology of the sediment core.
Taphonomic processes could also have affected the ability of sedDNA to
provide a reliable temporal record. For example, it was possible that
there was a delay in the time taken for cells in the surface water to
deposit in the sediment, particularly for smaller and more buoyant
cells. Recently deposited cells and DNA may have become resuspended
before complete burial and compaction within the sediment, and DNA may
have migrated between sediment layers which could have disrupted the
vertical organisation of DNA (Giguet-Covex et al ., 2019),
although it has been suggested that substantial DNA leaching between
layers is unlikely to occur in the permanently saturated sediments of
lakes (Anderson-Carpenter et al ., 2011).
Degradation of DNA over time could limit the reliability of sedDNA
reconstructions. Prior to 1970, the relative abundance of chlorophytes,
dinoflagellates, ochrophytes and bacillariophytes was low and stable in
the sedDNA record. Their occurrence in the microscopy record was also
relatively low prior to 1970, but there were indications of a slightly
higher occurrence in the earlier monitoring records between 1945 and
1950 which were not reflected in the sedDNA record. This could be
evidence of some DNA degradation and a reduced ability of sedDNA to
detect phytoplankton community change in older sediments. However,
separating the effect of DNA degradation from an increase in the
relative abundance of phytoplankton with intensification of nutrient
enrichment is complex as both factors could be expected to show a change
in the same direction (i.e., an increase from older to more recent
sediments). Heterotrophic eukaryotes that may have been active within
the sediment such as fungi were also sequenced with the 18S rRNA
amplicon primers, and their abundance within the sediment likely
contributed to the lower relative abundance of these phytoplankton
groups.
Cryptophytes were absent in the sedDNA record but were well-represented
in the microscopy-based record, and alloxanthin, the diagnostic pigment
of cryptophytes, was detected in the sediment core pigment record from
Esthwaite Water (Moorhouse et al ., 2018). Cryptophytes could
therefore be expected to be detected using sedDNA, but similar to the
present study, Capo et al . (2015) also reported that cryptophytes
were poorly represented by sedDNA and suggested that the absence of a
cell wall made their DNA vulnerable to degradation, and their high
nutritional content made them vulnerable to grazing by zooplankton so
that cells did not reach the sediment surface (Capo et al ., 2015;
Capo et al ., 2021). Haptophytes were also poorly represented by
sedDNA, and an underrepresentation of haptophytes in Lake Bourget,
France, as measured by sedDNA has previously been reported (Capoet al ., 2015). However, haptophyte temporal dynamics in an
Antarctic lake throughout the Holocene have successfully been
reconstructed using sedDNA (Coolen et al ., 2004), but the low
temperatures in the Antarctic lake may have promoted DNA preservation.
Haptophytes were not consistently counted throughout the monitoring
scheme, so determining whether this group was underrepresented because
they experienced greater rates of DNA degradation, or because they had a
low abundance in Esthwaite Water is challenging. The reliability of
sedDNA reconstructions depends on the extent of DNA degradation, which
may occur at varying rates for different taxa in different environments
(Capo et al ., 2021). Previous efforts have been made to explore
DNA degradation patterns in dinoflagellates and bacillariophytes in an
Antarctic lake core record (Boere et al ., 2011), and for
cyanobacterial taxa within microcosms (Mejbel et al ., 2021).
However, the extent of DNA degradation that different taxa may be
subject to in temperate lake sediments requires further research,
particularly for groups that were not well-represented by sedDNA, such
as cryptophytes and haptophytes.