Declines in ice cover are accompanied by light limitation responses and community change in freshwater diatoms

Abstract

The rediscovery of diatom blooms embedded within and beneath the Lake Erie ice cover (2007-2012) ignited interest in psychrophilic adaptations and winter limnology. Subsequent studies determined the vital role ice plays in winter diatom ecophysiology as diatoms partition to the underside of ice, thereby fixing their location within the photic zone. Yet, climate change has led to widespread ice decline across the Great Lakes, with Lake Erie presenting a nearly "ice-free" state in several recent winters. It has been hypothesized that the resultant turbid, isothermal water column induces light limitation amongst winter diatoms and thus serves as a competitive disadvantage. To investigate this hypothesis, we conducted a physiochemical and metatranscriptomic survey that spanned spatial, temporal, and climatic gradients of the winter Lake Erie water column (2019-2020). Our results suggest that ice-free conditions decreased planktonic diatom bloom magnitude and altered diatom community composition. Diatoms increased their expression of various photosynthetic genes and iron transporters, which suggests that the diatoms are attempting to increase their quantity of photosystems and light-harvesting components (a well-defined indicator of light limitation). We identified two gene families which serve to increase diatom fitness in the turbid ice-free water column: proton-pumping rhodopsins (a potential second means of light-driven energy acquisition) and fasciclins (a means to "raft" together to increase buoyancy and co-locate to the surface to optimize light acquisition). With large-scale climatic changes already underway, our observations provide insight into how diatoms respond to the dynamic ice conditions of today and shed light on how they will fare in a climatically altered tomorrow.

Keywords: Great Lakes; climate change; fasciclins; proton-pumping rhodopsins; winter limnology.

Figure 1

Climatic, spatial and temporal variability across Lake Erie samples. (A) MODIS satellite image (March 16th, 2014) depicting a large amount of ice cover across the Great Lakes. During the winter of 2014, Lake Erie had a mean annual ice cover of ~80%. (B) MODIS satellite image (February 12th, 2023) depicting a lack of ice cover across the Great Lakes. Sediment plumes can be observed throughout Lake Erie (the light brown coloration in the satellite image). During the winter of 2023, Lake Erie had a mean annual ice cover of ~8%. Figures adapted from data retrieved from the NOAA Great Lakes CoastWatch Node (NOAA 2023). (C) Sample sites across Lake Erie visited throughout winter-spring 2019 and 2020. (D) Historical trends in Lake Erie mean annual maximum ice cover (%). Open circles are years that (to our knowledge) do not have peer-reviewed published planktonic survey data. Solid black circles are years that were previously surveyed in prior published studies. Solid blue circles are years sampled in this study. Figure adapted from data retrieved from the NOAA GLERL database (NOAA-GLERL) [103].

Figure 2

Characterization of biotic community across Lake Erie sample sites. Samples are organized on the x-axis by season (W, winter; S, spring) and year. Solid shapes indicate the sample was collected during ice cover (2019) open shapes indicate the sample was collected during no ice cover (2020). Ice cover samples are indicated by a blue asterisk. (A) Total Chl a concentration of the whole water column community (i.e. >0.22 ) (g L⁻¹) (B) Chl a concentration of the large size fractioned community (i.e. >20 ) (g L⁻¹). (C) Cell abundances (cells⋅L⁻¹) of centric diatoms (Stephanodiscus spp. + A. islandica + small centric diatoms of 5–20 ). (D) Cell abundances of pennate diatoms (Fragilaria spp. + Asterionella formosa + Nitzschia spp). (E) Cell abundances (cells L⁻¹) of Stephanodiscus spp., Mediophyceae class. (F) Cell abundances (cells ⋅L⁻¹) of A. islandica, Coscinodiscophyceae class. Abbreviations: Chl a, chlorophyll a.

Figure 3

Relative transcript abundance of major eukaryotic phytoplankton taxa and diatom classes. Libraries are listed in chronological order of sample date on x-axes, with biological replicates joined by grey horizontal bars. Ice cover samples are indicated by a blue asterisk. (A) Relative transcript abundance of MEPT. All groups which formed <5% of the total mapped reads are included within “other” (Amoebozoa, Hilomonadea, Excavata, Rhizaria, not annotated [NA]). (B) Relative transcript abundance of Bacillariophyta classes Mediophyceae, Coscinodiscophyceae, Bacillariophyceae, Fragilariophyceae, and unclassified diatoms.

Figure 4

Dissimilarity (Bray-Curtis) clustering of the 20 metatranscriptomic library normalized expression values (TPM). (A) nMDS of the entire water column community expression, stress value = 0.063. (B) nMDS of the Bacillariophyta community expression, stress value = 0.050. Samples are presented as follows: February, squares; March, triangles; May, diamonds; June, circles. Blue indicates the sample was collected during the winter, black indicates the sample was collected during the spring. Solid shapes indicate the sample was collected during ice cover (2019) open shapes indicate the sample was collected during no ice cover (2020).

Figure 5

Bacillariophyta energy production and conversion transcript abundance patterns in response to ice cover. A) Taxonomic distribution of DE genes categorized within COG category C (energy production and conversion). (B) COG assignments for all 354 DE genes in response to ice cover, with COG category C indicated in blue. (C) Heatmap depicting COG category C DE gene expression (VST) in response to ice cover across the 14 winter libraries.

Figure 6

Bacillariophyta PPR transcript abundance patterns in response to ice. (A) Normalized expression (VST) of two DE genes functionally annotated as PPRs (PPR_1 [grey], PPR_2 [teal]) and representive DE genes functionally annotated to be involved in photosynthesis (black). Photosynthetic genes were selected because they encode for photosynthetic reaction centers (psbA, psbM) or the transfer of electrons along the photosystems (petF). Each circle corresponds to gene expression in one of the 14 libraries. Solid black circles indicate the sample was collected during ice cover (2019) open shapes indicate the sample was collected during no ice cover (2020). (B) Taxonomic distribution of the 11 genes functionally annotated as PPRs (and confirmed with subsequent phylogenetic analysis). (C) Phylogenetic tree of PPR distribution within diatoms. Putative rhodopsin-like proteins (n = 11, purple) were distributed within several rhodopsin groups and sub-groups to determine likelihood of putative genes being of bacterial or eukaryotic origins. The position of study genes is labelled by their associated groups, with the exception of genes 713 097 and 1 684 433 being GCPR transmembrane rhodopsin associated proteins, and gene 1 462 589 being unclear (most closely associated with the genes of metagenomic origin. Bootstrap values are based off 1000 replicates and are identified if above 80. Abbreviations: BACTERIORHO/EUK RHO-LIKE; bacteriorhodopsins and eukaryotic origin rhodopsin-like putative proteins, HALO; halorhodopsin, METAGENOME RHO-LIKE; metagenomic origin rhodopsin-like putative proteins, RHO-like; sensory eukaryotic rhodopsin-like proteins, XANTHO; xanthorhodopsin. The two DE PPRs are indicated with asterisks.

Figure 7

Bacillariophyta fasciclin transcript abundance patterns in response to ice cover. (A) Taxonomic distribution of DE genes categorized within COG category M (cell wall, membrane, envelope biogenesis). (B) COG assignments for all 354 DE genes in response to ice cover, with COG category M indicated in blue. (C) Heatmap depicting COG category M DE gene expression (VST) in response to ice cover across the 14 winter libraries. (D) Phylogenetic tree of fasciclin distribution within diatoms. Bootstrap values above 70 are indicated with black lines. The FAS1 domain was found in 141 marine and freshwater diatoms of diverse ecological habitats (indicated in blue). The 18 DE diatom fasciclins in this study are indicated in purple with asterisks. Bacterial fasciclins are indicated in dark green, with cyanobacteria (pink), chytrids (red), other algae (purple), and other eukaryotes (light green).

Figure 8

Schematic representation of how ice cover alters freshwater diatom colocation strategy throughout the water column. (A) Ice-covered water column exhibiting minimal convective mixing. As a result, I_k < I_wc (where I_k = irradiance at which photosynthesis is light saturated and I_wc = mean water column irradiance). I_wc is calculated based on light extinction coefficient and mixing depth, which in an ice-free winter (i.e. holomictic state) is the bottom, while in the presence of ice-cover, is limited to shallow convective mixing. Diatoms partition to the surface ice cover within the photic zone. (B) Ice-free water column which exhibits isothermal conditions and thorough mixing. As a result, I_k > I_wc, and light-limited diatoms express fasciclins to form rafts of increased buoyancy to optimize their ability to harvest light in the turbid water column. Beige colored diatoms in both diagrams represent diatoms that possess PPRs, with an increased number of PPR-possessing diatoms selected for in the ice-free turbid water column in panel B.