Title: 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. more »« less
Zepernick, Brittany N.; Denison, Elizabeth R.; Chaffin, Justin D.; Bullerjahn, George S.; Pennacchio, Christa P.; Frenken, Thijs; Peck, Daniel H.; Anderson, James T.; Niles, Derek; Zastepa, Arthur; et al
(, Microbiology Resource Announcements)
Rokas, Antonis
(Ed.)
ABSTRACT Previous reports suggest planktonic and under-ice winter microbial communities in Lake Erie are dominated by diatoms. Here, we report the assembled metatranscriptomes of 79 Lake Erie surface water microbial communities spanning both the winter (28 samples) and spring (51 samples) months over spatial, temporal, and climatic gradients in 2019 through 2020.
Zepernick, Brittany N.; Gann, Eric R.; Martin, Robbie M.; Pound, Helena L.; Krausfeldt, Lauren E.; Chaffin, Justin D.; Wilhelm, Steven W.
(, Frontiers in Microbiology)
null
(Ed.)
Cyanobacterial Harmful Algal Blooms (CyanoHABs) commonly increase water column pH to alkaline levels ≥9.2, and to as high as 11. This elevated pH has been suggested to confer a competitive advantage to cyanobacteria such as Microcystis aeruginosa . Yet, there is limited information regarding the restrictive effects bloom-induced pH levels may impose on this cyanobacterium’s competitors. Due to the pH-dependency of biosilicification processes, diatoms (which seasonally both precede and proceed Microcystis blooms in many fresh waters) may be unable to synthesize frustules at these pH levels. We assessed the effects of pH on the ecologically relevant diatom Fragilaria crotonensis in vitro , and on a Lake Erie diatom community in situ . In vitro assays revealed F. crotonensis monocultures exhibited lower growth rates and abundances when cultivated at a starting pH of 9.2 in comparison to pH 7.7. The suppressed growth trends in F. crotonensis were exacerbated when co-cultured with M. aeruginosa at pH conditions and cell densities that simulated a cyanobacteria bloom. Estimates demonstrated a significant decrease in silica (Si) deposition at alkaline pH in both in vitro F. crotonensis cultures and in situ Lake Erie diatom assemblages, after as little as 48 h of alkaline pH-exposure. These observations indicate elevated pH negatively affected growth rate and diatom silica deposition; in total providing a competitive disadvantage for diatoms. Our observations demonstrate pH likely plays a significant role in bloom succession, creating a potential to prolong summer Microcystis blooms and constrain diatom fall resurgence.
Zepernick, Brittany N.; Niknejad, David J.; Stark, Gwendolyn F.; Truchon, Alexander R.; Martin, Robbie M.; Rossignol, Karen L.; Paerl, Hans W.; Wilhelm, Steven W.
(, Frontiers in Microbiology)
Harmful algal blooms (HABs) caused by the toxin-producing cyanobacteria Microcystis spp., can increase water column pH. While the effect(s) of these basified conditions on the bloom formers are a high research priority, how these pH shifts affect other biota remains understudied. Recently, it was shown these high pH levels decrease growth and Si deposition rates in the freshwater diatom Fragilaria crotonensis and natural Lake Erie (Canada-US) diatom populations. However, the physiological mechanisms and transcriptional responses of diatoms associated with these observations remain to be documented. Here, we examined F. crotonensis with a set of morphological, physiological, and transcriptomic tools to identify cellular responses to high pH. We suggest 2 potential mechanisms that may contribute to morphological and physiological pH effects observed in F. crotonensis . Moreover, we identified a significant upregulation of mobile genetic elements in the F. crotonensis genome which appear to be an extreme transcriptional response to this abiotic stress to enhance cellular evolution rates–a process we have termed “ genomic roulette. ” We discuss the ecological and biogeochemical effects high pH conditions impose on fresh waters and suggest a means by which freshwater diatoms such as F. crotonensis may evade high pH stress to survive in a “basified” future.
Denison, Elizabeth R; Zepernick, Brittany N; McKay, R_Michael L; Wilhelm, Steven W
(, mSystems)
Blanchard, Jeffrey Lawrence
(Ed.)
ABSTRACT Winter is a relatively under-studied season in freshwater ecology. The paucity of wintertime surveys has led to a lack of knowledge regarding microbial community activity during the winter in Lake Erie, a North American Great Lake. Viruses shape microbial communities and regulate biogeochemical cycles by acting as top-down controls, yet very few efforts have been made to examine active virus populations during the winter in Lake Erie. Furthermore, climate change-driven declines in seasonal ice cover have been shown to influence microbial community structure, but no studies have compared viral community activity between different ice cover conditions. We surveyed surface water metatranscriptomes for viral hallmark genes as a proxy for active virus populations and compared activity metrics between ice-covered and ice-free conditions from two sampled winters. Transcriptionally active viral communities were detected in both winters, spanning diverse phylogenetic clades of putative bacteriophage (Caudoviricetes), giant viruses (Nucleocytoviricota, or NCLDV), and RNA viruses (Orthornavirae). However, viral community activity metrics revealed pronounced differences between the ice-covered and ice-free winters. Viral community composition was distinct between winters and viral hallmark gene richness was reduced in the ice-covered relative to the ice-free conditions. In addition, the observed differences in viral communities correlated with microbial community activity metrics. Overall, these findings contribute to our understanding of the viral populations that are active during the winter in Lake Erie and suggest that viral community activity may be associated with ice cover extent.IMPORTANCEAs seasonal ice cover is projected to become increasingly rare on large temperate lakes, there is a need to understand how microbial communities might respond to changing ice conditions. Although it is widely recognized that viruses impact microbial community structure and function, there is little known regarding wintertime viral activity or the relationship between viral activity and ice cover extent. Our metatranscriptomic analyses indicated that viruses were transcriptionally active in the winter surface waters of Lake Erie. These findings also expanded the known diversity of viral lineages in the Great Lakes. Notably, viral community activity metrics were significantly different between the two sampled winters. The pronounced differences we observed in active viral communities between the ice-covered and ice-free samples merit further research regarding how viral communities will function in future, potentially ice-free, freshwater systems.
Dawson, H M; Heal, K R; Torstensson, A; Carlson, L T; Ingalls, A E; Young, J N
(, Integrative and Comparative Biology)
null
(Ed.)
Synopsis Intense bottom-ice algal blooms, often dominated by diatoms, are an important source of food for grazers, organic matter for export during sea ice melt, and dissolved organic carbon. Sea-ice diatoms have a number of adaptations, including accumulation of compatible solutes, that allows them to inhabit this highly variable environment characterized by extremes in temperature, salinity, and light. In addition to protecting them from extreme conditions, these compounds present a labile, nutrient-rich source of organic matter, and include precursors to climate active compounds (e.g., dimethyl sulfide [DMS]), which are likely regulated with environmental change. Here, intracellular concentrations of 45 metabolites were quantified in three sea-ice diatom species and were compared to two temperate diatom species, with a focus on compatible solutes and free amino acid pools. There was a large diversity of metabolite concentrations between diatoms with no clear pattern identifiable for sea-ice species. Concentrations of some compatible solutes (isethionic acid, homarine) approached 1 M in the sea-ice diatoms, Fragilariopsis cylindrus and Navicula cf. perminuta, but not in the larger sea-ice diatom, Nitzschia lecointei or in the temperate diatom species. The differential use of compatible solutes in sea-ice diatoms suggests different adaptive strategies and highlights which small organic compounds may be important in polar biogeochemical cycles.
Zepernick, Brittany_N, Chase, Emily_E, Denison, Elizabeth_R, Gilbert, Naomi_E, Truchon, Alexander_R, Frenken, Thijs, Cody, William_R, Martin, Robbie_M, Chaffin, Justin_D, Bullerjahn, George_S, McKay, R_Michael_L, and Wilhelm, Steven_W.
"Declines in ice cover are accompanied by light limitation responses and community change in freshwater diatoms". The ISME Journal 18 (1). Country unknown/Code not available: Oxford University Press. https://doi.org/10.1093/ismejo/wrad015.https://par.nsf.gov/biblio/10492708.
@article{osti_10492708,
place = {Country unknown/Code not available},
title = {Declines in ice cover are accompanied by light limitation responses and community change in freshwater diatoms},
url = {https://par.nsf.gov/biblio/10492708},
DOI = {10.1093/ismejo/wrad015},
abstractNote = {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.},
journal = {The ISME Journal},
volume = {18},
number = {1},
publisher = {Oxford University Press},
author = {Zepernick, Brittany_N and Chase, Emily_E and Denison, Elizabeth_R and Gilbert, Naomi_E and Truchon, Alexander_R and Frenken, Thijs and Cody, William_R and Martin, Robbie_M and Chaffin, Justin_D and Bullerjahn, George_S and McKay, R_Michael_L and Wilhelm, Steven_W},
}
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