Evolution of Predicted Acid Resistance Mechanisms in the Extremely Acidophilic Leptospirillum Genus

Abstract

Organisms that thrive in extremely acidic environments (≤pH 3.5) are of widespread importance in industrial applications, environmental issues, and evolutionary studies. Leptospirillum spp. constitute the only extremely acidophilic microbes in the phylogenetically deep-rooted bacterial phylum Nitrospirae. Leptospirilli are Gram-negative, obligatory chemolithoautotrophic, aerobic, ferrous iron oxidizers. This paper predicts genes that Leptospirilli use to survive at low pH and infers their evolutionary trajectory. Phylogenetic and other bioinformatic approaches suggest that these genes can be classified into (i) “first line of defense”, involved in the prevention of the entry of protons into the cell, and (ii) neutralization or expulsion of protons that enter the cell. The first line of defense includes potassium transporters, predicted to form an inside positive membrane potential, spermidines, hopanoids, and Slps (starvation-inducible outer membrane proteins). The “second line of defense“ includes proton pumps and enzymes that consume protons. Maximum parsimony, clustering methods, and gene alignments are used to infer the evolutionary trajectory that potentially enabled the ancestral Leptospirillum to transition from a postulated circum-neutral pH environment to an extremely acidic one. The hypothesized trajectory includes gene gains/loss events driven extensively by horizontal gene transfer, gene duplications, gene mutations, and genomic rearrangements.

Recent progress in the application of omics technologies in the study of bio-mining microorganisms from extreme environments

“…Predicted models of carbon assimilation, nitrogen metabolism and sulfur oxidation in A. thiooxidans strains have been reported [34]. The acid resistance model in Leptospirillum is mainly divided into the first line of defense that prevents the uptake of protons into the cell and second line of defense that neutralizes or expels the protons that enter the cell [35]. However, there are still uncertain factors in the model, such as the unknown function of the genes encoding orphan hypothetical proteins.…”

Genomic Analysis of a Newly Isolated Acidithiobacillus ferridurans JAGS Strain Reveals Its Adaptation to Acid Mine Drainage

“…In response to acidic heavy metal stress, acidophiles have developed different genetic mechanisms to survive and they are described, which can be very complex [43,44]. The metabolic diversity and adaptive mechanisms of Acidithiobacillus spp.…”

Extremophilic Microorganisms for the Treatment of Toxic Pollutants in the Environment

“…Acidophilic microorganisms can survive under extremely low pH (less than pH 3) conditions, maintaining pH homeostasis by controlling proton permeation [ 19 ]. For example, microorganisms from the genera Thermoplasma , Ferroplasma, and Sulfolobus can regulate proton permeation under extremely low pH conditions due to a highly impermeable cell membrane mainly composed of tetraether lipids having a diverse array of polar head groups and a bulky isoprenoid core [ 20 , 21 , 22 , 23 ]. The modulation of the influx of protons through the proton pump system is important to survive at low pH, and putative proton pump proteins such as H + -ATPase, symporters, and antiporters from Ferroplasma type II and Leptospirillium group II are involved in maintaining pH homeostasis [ 21 , 24 , 25 ].…”

“…For example, microorganisms from the genera Thermoplasma , Ferroplasma, and Sulfolobus can regulate proton permeation under extremely low pH conditions due to a highly impermeable cell membrane mainly composed of tetraether lipids having a diverse array of polar head groups and a bulky isoprenoid core [ 20 , 21 , 22 , 23 ]. The modulation of the influx of protons through the proton pump system is important to survive at low pH, and putative proton pump proteins such as H + -ATPase, symporters, and antiporters from Ferroplasma type II and Leptospirillium group II are involved in maintaining pH homeostasis [ 21 , 24 , 25 ]. Moreover, F 0 F 1 -type adenosine triphosphate synthase in Bacillus acidocaldarus , Thermoplasma acidophilum , and Leptospirillium ferriphilum is known to play a critical role in regulating proton permeation [ 25 ].…”