Extremophilic models for astrobiology: haloarchaeal survival strategies and pigments for remote sensing

Abstract

Recent progress in extremophile biology, exploration of planetary bodies in the solar system, and the detection and characterization of extrasolar planets are leading to new insights in the field of astrobiology and possible distribution of life in the universe. Among the many extremophiles on Earth, the halophilic Archaea (Haloarchaea) are especially attractive models for astrobiology, being evolutionarily ancient and physiologically versatile, potentially surviving in a variety of planetary environments and with relevance for in situ life detection. Haloarchaea are polyextremophilic with tolerance of saturating salinity, anaerobic conditions, high levels of ultraviolet and ionizing radiation, subzero temperatures, desiccation, and toxic ions. Haloarchaea survive launches into Earth's stratosphere encountering conditions similar to those found on the surface of Mars. Studies of their unique proteins are revealing mechanisms permitting activity and function in high ionic strength, perchlorates, and subzero temperatures. Haloarchaea also produce spectacular blooms visible from space due to synthesis of red-orange isoprenoid carotenoids used for photoprotection and photorepair processes and purple retinal chromoproteins for phototrophy and phototaxis. Remote sensing using visible and infrared spectroscopy has shown that haloarchaeal pigments exhibit both a discernable peak of absorption and a reflective "green edge". Since the pigments produce remotely detectable features, they may influence the spectrum from an inhabited exoplanet imaged by a future large space-based telescope. In this review, we focus primarily on studies of two Haloarchaea, Halobacterium sp. NRC-1 and Halorubrum lacusprofundi.

Keywords: Astrobiology; Biosignature; Haloarchaea; Phototrophy; Polyextremophile; Purple membrane; Retinal.

Fig. 1.. Isoelectric point distribution of haloarchaeal and non-haloarchaeal proteins.

Percent of total proteins with pI values are plotted versus pI for the Haloarchaea, Halobacterium sp. NRC-1 (gray) and Halorubrum lacusprofundi (dark blue), and non-halophiles, E. coli (medium blue), Bacillus subtilis (light blue), Methanocaldococcus jannaschii (red) and Schizosaccharomyces pombe (green) (DasSarma and DasSarma 2015;Kennedy, et al. 2001).

Fig. 2.. Distribution of haloarchaeal orthologous groups.

Haloarchaeal orthologous groups (HOGs) identified by reciprocal Blast analysis exhibit a bimodal distribution, with the largest number of proteins with unknown function and no associated Clusters of Orthologous Groups (COGs) shown in blue. Those with known or predictable function present in haloarchaeal proteomes are shown in other colors (orange, green, reddish brown, and purple) with functions indicated on the right (Capes, et al. 2012).

Fig. 3.. Pigment biosynthesis in Haloarchaea.

Biosynthesis of common pigments in Haloarchaea such as Halobacterium species proceeds from acetate via mevalonate to lycopene where the pathway splits to form the bacterioruberins or β-carotene and retinal. Bacterioruberins have been implicated in photoprotection and repair while retinal acts as the chromophore in purple membrane used for phototrophic growth (DasSarma, et al. 2001).

Fig. 4.. Phototrophic capability of Haloarchaea.

Haloarchaea such as Halobacterium sp. NRC-1 contain the retinal protein bacteriorhodopsin (BR) which is an outwardly directed light-driven proton pump producing a proton-motive gradient that drives ATP synthesis using ADP and P_i (left). Trimers of BR form a hexagonal lattice in the membrane (circular inset, center). BR’s seven transmembrane α-helical segments are shown in ribbon form (right) with the bound retinal (stick structure) involved in promoting transport of protons (H⁺ ions) across the membrane (DasSarma and Schwieterman 2019).

Fig. 5.. Reflective green edge from haloarchaeal pigments.

A laboratory reflection spectrum of H. lacusprofundi (top panel) and an environmentally characterized halophile bloom under a simulated Earth atmosphere (bottom panel), including atmospheric absorption and scattering, are shown, plotting wavelength in nanometers (nm) (abscissa) versus percent reflectivity (ordinate) (DasSarma and Schwieterman 2019). Dashed lines are shown for reference and strong water (H₂O) and oxygen (O₂) interference bands labeled.