Morphological, physiological, and transcriptional responses of the freshwater diatom Fragilaria crotonensis to elevated pH conditions

Abstract

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.

A tale of two blooms: do ecological paradigms for algal bloom success and succession require revisiting?

“…Yet, there remains a forgotten exception to this trend; prolific summer Fragilaria crotonensis blooms have been reported across the western basin of Lake Erie throughout the late 1960’s and into the early 2000’s (coinciding with the rejuvenation of Lake Erie), with concentrations of this chain-forming diatom reported as high as 950,000 filaments L −1 ( Beeton, 1965 ; Gladish and Munawar, 1980 ; Hartig, 1987 ; Munawar et al, 2008 ; Munawar and Munawar, 1976 ). To date, this genus remains a prominent member of the Lake Erie summer water column ( Bramburger and Reavie, 2016 ; Chaffin et al, 2019 ; Reavie et al, 2014 ; Saxton et al, 2012 ), though studies concerning its ecological success are limited ( Hartig, 1987 ; Hartig and Wallen, 1986 ; Zepernick et al, 2021 ; Zepernick et al, 2022b ). Cumulatively, the data indicate populations of diatoms are routinely abundant in the summer water column of Lake Erie regardless of shifts in trophic status and nutrient availability, yet these diatoms receive little recognition.…”

“…In contrast to atmospheric driven lake acidification across decades, biologically driven lake basification occurs on a diel and seasonal basis ( Zepernick et al, 2021 ; Zepernick et al, 2022b ). Microcystis spp.…”

“…Novel data has suggested a need for a better understanding of phytoplankton competition and the role of additional drivers in algal success and succession. For example, recent research has characterized a role of cyanobacterial-induced elevated pH in the water column ( i.e., lake basification) in algal competition and succession ( Shapiro, 1990 ; Zepernick et al, 2021 ; Zepernick et al, 2022b ). Beyond biologically-driven lake basification, it has been projected anthropogenically-driven lake acidification may occur at the same rate as ocean acidification ( Phillips et al, 2015 ).…”

Transcriptional responses to salinity‐induced changes in cell wall morphology of the euryhaline diatom Pleurosira laevis

“…Transposable elements are known to become active under environmental changes or stress conditions (Casacuberta & González, 2013). In diatoms, up-regulation of TEs has been reported in response to thermal stress (Egue et al, 2015), high biomass density (Oliver et al, 2010), and elevated pCO 2 (Huang et al, 2019) in Phaeodactylum tricornutum, elevated pH in Fragilaria crotonensis (Zepernick et al, 2022), presence of grazers in Skeletonema marinoi (Amato et al, 2018), and cold stress in Leptocylindrus aporus (Pargana et al, 2019). In Pinseel et al (2022), a lower salinity condition triggered the down-regulation of TEs in S. marinoi.…”

Functional stress responses in Glaucophyta: evidence of ethylene and abscisic acid functions inCyanophora paradoxa

“…In the yeast Saccharomyces cerevisiae, the protein RIO1 is required for cell cycle progression (Angermayr et al, 2002), and the protein is known to interact with the ribosome, influencing translation (LaRonde- LeBlanc and Wlodawer, 2005). Moreover, a RIO1 homolog was identified as an upregulated gene under elevated pH, a condition associated with decreased growth, in the diatom Fragilaria crotonensis (Zepernick et al, 2022). It is not clear how the upregulation of a protein kinase needed for cell cycle progression influences the observed growth arrest.…”