Declines in ice cover induce light limitation in freshwater diatoms

Abstract The rediscovery of diatom blooms embedded within and beneath Lake Erie ice cover (2007-2012) ignited an intense interest in psychrophilic adaptations and winter limnology. Subsequent studies determined ice plays a vital role 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 the resultant turbid, isothermal water column will induce light limitation amongst winter diatoms, serving as a detrimental competitive disadvantage. Here, we conducted a physiochemical and metatranscriptomic survey of the winter Lake Erie water column (2019-2020) that spanned spatial, temporal, and climatic gradients to investigate this hypothesis. We determined ice-free conditions decreased diatom bloom magnitude and altered diatom community composition. Diatoms increased the expression of various photosynthetic genes and iron transporters, suggesting they are attempting to increase their quantity of photosystems and light-harvesting components (a well-defined indicator of light limitation). Notably, we identified two gene families which serve to increase diatom fitness in the turbid ice-free water column: proton-pumping rhodopsins (a 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.