Transcriptomic analysis reveals how a lack of potassium ions increases Sulfolobus acidocaldarius sensitivity to pH changes

Abstract

Extremely acidophilic microorganisms (optimum growth pH of 3) maintain a near neutral cytoplasmic pH via several homeostatic mechanisms, including an inside positive membrane potential created by potassium ions. Transcriptomic responses to pH stress in the thermoacidophilic archaeon, Sulfolobus acidocaldarius were investigated by growing cells without added sodium and/or potassium ions at both optimal and sub-optimal pH. Culturing the cells in the absence of added sodium or potassium ions resulted in a reduced growth rate compared to full-salt conditions as well as 43 and 75 significantly different RNA transcript ratios, respectively. Differentially expressed RNA transcripts during growth in the absence of added sodium ions included genes coding for permeases, a sodium/proline transporter and electron transport proteins. In contrast, culturing without added potassium ions resulted in higher RNA transcripts for similar genes as a lack of sodium ions plus genes related to spermidine that has a general role in response to stress and a decarboxylase that potentially consumes protons. The greatest RNA transcript response occurred when S. acidocaldarius cells were grown in the absence of potassium and/or sodium at a sub-optimal pH. These adaptations included those listed above plus osmoregulated glucans and mechanosensitive channels that have previously been shown to respond to osmotic stress. In addition, data analyses revealed two co-expressed IclR family transcriptional regulator genes with a previously unknown role in the S. acidocaldarius pH stress response. Our study provides additional evidence towards the importance of potassium in acidophile growth at acidic pH.

Hyperdiverse archaea near life limits at the polyextreme geothermal Dallol area

“…This suggests that molecular adaptations to simultaneous low-pH and high-salt extremes are incompatible beyond those limits. In principle, more acidic proteins, intracellular K + accumulation (salt-in strategy) or internal positive membrane potential generated by cations or H + /cation antiporters serve both acidophilic 15 and halophilic adaptations (33)(34)(35). However, membrane stability/function problems and/or high external Clconcentrations inducing H + and cation (K + /Na + ) import and potentially disrupting membrane bioenergetics (34), might be deleterious under these conditions.…”

Biological Membranes in Extreme Conditions: Anionic Tetraether Lipid Membranes and Their Interactions with Sodium and Potassium

“…24 Under highly acidic pH, many of the membrane binding sites are neutralized by protons, making it more difficult for the archaea to scavenge for alkali cations that are necessary for their growth. 33 Thus, the antenna effect is non-operative or less efficient at high acidity, where the concentration of protons is higher than that of alkali cations.…”

“…24 To be able to sustain growth under such conditions, these organisms must have evolved an efficient mechanism to pump ions into their cytoplasms. Cations transporters are essential for this, but these proteins must be able to gather the scarce ions from the extracellular environment.…”

“…23 In addition, recent RNA transcript profiling revealed that this archaeon has different expression profiles depending on the cation and pH. 24 In this study we used MD simulations to analyze the interactions of GDNT membranes and Na + or K + solutions at different concentrations.…”

Peer Review #2 of "Two membrane-bound transcription factors regulate expression of various type-IV-pili surface structures in Sulfolobus acidocaldarius (v0.1)"

“…For instance, in Methanocaldococcus jannaschii hydrogen limitation promotes archaella synthesis while in M. maripaludis a decrease of archaellum gene transcription in response to leucine starvation was described (Mukhopadhyay, Johnson & Wolfe, 2000;Hendrickson et al, 2008). It is known that under different stress sources, such as nutrient or phosphate limitation or osmotic and pH stress, S. acidocaldarius regulates gene transcription and translation according to its needs (Osorio & Jerez, 1996;Lassak et al, 2012Lassak et al, , 2013Buetti-Dinh et al, 2016). To date, neither arnR nor arnR1 were regulated under conditions other than starvation (e.g pH and salt-stress,(Buetti-Dinh et al, 2016)), raising the question of which membrane-related signal both regulators sense and transduce.…”