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.
