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 Lake Erie ice cover (2007-2012) ignited 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. Our results suggest ice-free conditions decreased planktonic 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). We identified two gene families which serve to increase diatom fitness in the turbid ice-free water column: proton-pumping rhodopsins (PPRs; 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.

Metatranscriptomics reveals declines in ice cover influence winter viral community activity

“…Our findings suggest the observed differences in active viral communities reflect the ice cover-driven shifts in microbial community structure. Similar to previous observations (31, 49), we observed evidence of a decrease in magnitude of the winter diatom bloom in the ice-free conditions compared to the ice-covered state. It is unclear the degree that host population structure influences winter viral communities, but the differences in host representation and diversity between the ice-covered and ice-free states are in part responsible.…”

“…Collectively, viral hallmark genes comprised a larger portion of the ice-free communities ( i.e., total TPM) compared to the ice-covered (Figure 3A). Higher viral abundance in the ice-free conditions coincided with lower abundance of the bloom-forming diatoms ( Bacillariophyta ), both in terms of lower diatom transcript abundance (Figure 3B) and cell counts (49). Conversely, prokaryotic transcripts had higher representation in the ice-free conditions (13-36% versus 30-67%, respectively) (Figure 3B).…”

“…Light availability has been implicated as a driving factor behind how declining ice cover shapes microbial communities (94), specifically regarding phytoplankton ecology in Lake Erie (31, 49). Furthermore, viruses can encode functional metabolic genes involved in phototrophy and light-sensing, namely the D1 protein (PsbA) in cyanophage (95) and rhodopsin in NCLDV (96).…”

“…This study used the metatranscriptome co-assembly and gene predictions generated by Zepernick et al . (49). Briefly, in Zepernick et al ., quality-filtered reads were co-assembled using MEGAHIT v1.2.9 (50) and the resulting co-assembly was assessed using QUAST v5.0.2 (Table S1) (51).…”

“…Taxonomic and functional annotation of predicted cellular genes were retrieved from Zepernick et al . (49). Briefly, taxonomy was estimated using EUKulele v1.0.6 (83), where protein sequences were aligned to the PhyloDB database v1.076 by DIAMOND BLASTp.…”