Eurypsychrophilic acidophiles: From (meta)genomes to low-temperature biotechnologies

Abstract

Low temperature and acidic environments encompass natural milieus such as acid rock drainage in Antarctica and anthropogenic sites including drained sulfidic sediments in Scandinavia. The microorganisms inhabiting these environments include polyextremophiles that are both extreme acidophiles (defined as having an optimum growth pH < 3), and eurypsychrophiles that grow at low temperatures down to approximately 4°C but have an optimum temperature for growth above 15°C. Eurypsychrophilic acidophiles have important roles in natural biogeochemical cycling on earth and potentially on other planetary bodies and moons along with biotechnological applications in, for instance, low-temperature metal dissolution from metal sulfides. Five low-temperature acidophiles are characterized, namely, Acidithiobacillus ferriphilus, Acidithiobacillus ferrivorans, Acidithiobacillus ferrooxidans, "Ferrovum myxofaciens," and Alicyclobacillus disulfidooxidans, and their characteristics are reviewed. Our understanding of characterized and environmental eurypsychrophilic acidophiles has been accelerated by the application of "omics" techniques that have aided in revealing adaptations to low pH and temperature that can be synergistic, while other adaptations are potentially antagonistic. The lack of known acidophiles that exclusively grow below 15°C may be due to the antagonistic nature of adaptations in this polyextremophile. In conclusion, this review summarizes the knowledge of eurypsychrophilic acidophiles and places the information in evolutionary, environmental, biotechnological, and exobiology perspectives.

Keywords: acidic (microbial) environments; astrobiology; bio-applications; polyextremophile; snowball earth; stenopsychrophile.

Figure 1

Acidic and low-temperature environments. Clockwise from top left: Mars and moons of Saturn and Jupiter (modified from Wikipedia CC BY-SA 3.0 IGO); boreal AS soil (ASS) created by land uplift (courtesy Eva Högfors-Rönnholm); high altitude lake (modified from Wikipedia public domain image); mining of metal sulfides at, e.g., high altitudes; AMD from under ice sulfide tailings seepage ponds; a low-temperature AMD stream in an underground mine; low-temperature caves (modified photograph by Dave Bunnell from Wikipedia CC BY-SA 2.5); black smokers releasing sulfides (modified from Wikipedia public domain image); and ARD from sulfide minerals, e.g., Antarctica (credit Ángeles Aguilera, Bernhard Dold, and Elena González-Toril), reproduced with permission.

Figure 2

Maximum likelihood phylogenetic tree of eurypsychrophilic acidophiles (in blue) plus relatives. The tree was constructed using 31 conserved proteins (Ciccarelli et al., 2006) using 1,000 replicates. Bootstrap values of ≥60% are represented by black dots on the nodes. The phylogenomic tree was visualized with iTOL6 (Letunic and Bork, 2021).

Figure 3

Plot of pH vs. temperature optima and ranges of characterized eurypsychrophilic acidophiles with the limits of low-temperature growth and extreme acidophiles are shaded in blue. The species are A. ferrivorans strains (all in black) from top to bottom NO-37, CF27, SS3, and ACH; At. ferrooxidans PG05 and MC2.2 represented as a single line (blue); “F. myxofaciens” P3G (orange); and A. ferriphilus M20 (green). The strains with an optimum pH of 2.5 were slightly adjusted for visual clarity.

Figure 4

Acidophile and low-temperature adaptations for selected genomes based upon complete genomes and type strains of the available species. Data used during the preparation of the figure were drawn from the AciDB database of acidophilic organisms (Neira et al., 2020).