Journal of Astrobiology and Space Science Reviews, 1, 235--241, 2019
Richard A. Armstrong
Vision Sciences, Aston University, Birmingham B4 7ET, UK
Key Words: Extremophile, Endolithic lichen, Dibaeis baeomyces, Ascomycota, Basidiomycota
A significant assertion of the publication by Joseph et al. (2019) (“Evidence for Life on Mars”) is the claim that lichens and their symbionts may have colonized Mars. Lichens are often described as 'extremophiles', a testament to their ability to adapt and thrive in some of the most extreme environments on Earth including deserts, at the poles and at high altitudes (Armstrong 2017). Given this reputation, it is not surprising that they are regarded as organisms that could potentially survive on Mars (Armstrong 2004). In particular, the paper by Joseph et al (2019) publishes images resembling 'podetia' (reproductive stalks) similar to those of the Earth lichen Dibaeis baeomyces (Brodo 2001). This commentary critically reviews this assertion with evidence for and against and also discusses the implications for lichenology if the claims were ultimately shown to be true.
Mars is an inhospitable, barren, and rocky planet unprotected from UV light and subjected to freezing temperatures and frequent sandstorms. Daytime surface temperatures may vary from 26.6°C during rare sunny days to -93°C at the poles in winter, air temperature rarely rising above zero and decreasing markedly with altitude above the surface. The Martian atmosphere is composed mainly of carbon dioxide (CO2) with trace quantities of nitrogen, argon, oxygen, and carbon monoxide (Nier et al. 2003). Moisture levels are extremely low in the atmosphere, spectroscopic observations suggesting one thousandth of that in the atmosphere above the Sahara desert on Earth. Subsequent studies using theoretical climate models and experiments on Earth which simulate Martian environments (Kuznetz and Gan 2002) suggest that liquid water may be stable for extended periods of time on the Martian surface under present-day conditions (Titus et al 2003). Air pressure is approximately 1% of that of Earth and wind speeds recorded at the Viking Lander site were 2 -7 m s-1 but under conditions of low gravity could rise to 17 -30 m s-1 during dust storms. Lichens could fulfill some of the requirements for growing in this environment.
Lichen adaptation to space conditions has been investigated in a series of experiments carried out at the European Biopan facility (Raggio et al. 2011) and the International Space Station (ISS) (Brandt et al. 2015, 2016). Lichens in space are exposed to the combined effects of insolation, UV irradiation, cosmic radiation, extreme low temperatures, and a vacuum (Brandt et al. 2015). Hence, after long-term exposure of 559 days to these conditions, the foliose lichen Xanthoria elegans showed considerable resistance with post-exposure activity at 50-80% of normal in the alga and 60-90% in the fungus (Brandt et al. 2015). Growth and proliferation of isolated algal cells was demonstrated after all exposures. In addition, photosynthetic activity has been demonstrated post-exposure with high viability of algal cells and low rates of photosynthetic impairment (Meesen et al. 2014). However, strong impairment of photosynthesis and photo-protective mechanisms were also observed when the isolated alga were irradiated emphasizing the importance of protection within the lichen to survive very dry conditions (Meesen et al. 2014). By contrast, in Aspicilia fruticulosa --during a 10 day spaceflight-- solar electromagnetic radiation exposure between 100 - 200 nm caused reductions in chlorophyll 'a' yield, a reduction which recovered after 72 hours reactivation, indicative of the lichens capability of repairing space damage (Raggio et al. 2011).
Detailed examination of images of the Martian surface has led to claims of the presence of 'lichen-like' structures (Dass 2017; Joseph 2014; Rabb 2018; Small 2018). In the paper of Joseph et al (2019), some of these images resemble the reproductive podetia of D. baeomyces, a species with similarities to Icmadophila ericetorum and several species of the genus Baeomyces and some Cladonia species. The algal partner of D. baeomyces is probably the green alga Coccomyxa and on earth D. baeomyces colonizes unstable soil, loose sand, and dry clay in full sun, disturbed ground being preferred. The species is a lichenized member of the ascomycota and the apothecia containing the asci and spores are 1-4 mm on podetia up to 6 mm long, similar to those revealed in Martian images (Joseph et al. 2019).
Observations in extreme environments on Earth have suggested that lichens could also live within rocks on Mars ('endolithic lichens'). Hence, dehydrated Antarctic crypto-endolithic communities and colonies of rock inhabiting black fungi were exposed to simulated Martian conditions for 18 months at the ISS (Onofri et al. 2015), less than 10% of the colonies proliferated while 60% of cells and rock communities remained intact. Endolithic lichens on Mars may be able to better tolerate the low temperatures of the surface and as in the dry valleys of Antarctica, the rock subsurface is likely to be warmer and subjected to smaller fluctuations than the surface of the rocks. Nevertheless, the lack of a ready supply of surface water would be a significant problem for these lichens.
It is a possibility, however, that in certain areas, water ice on the surface may melt and penetrate the boulders, the lichens remaining in a dehydrated condition during the long intervening periods. In Antarctica, CO2 exchange takes place very slowly through a relatively thick surface crust (Kappen and Friedmann 1983) and this could presumably also take place in Martian rocks. In addition, in regions of high light intensity, approximately 1% of the light reaches the lichen zone inside Antarctic rocks, the harmful UV being screened out by the dark-pigmented fungal layer and this process would be even more important on Mars. The main source of nitrogen for endolithic lichens is abiotically fixed nitrogen by atmospheric electric discharge, the fixed nitrogen then being conveyed to the rock by atmospheric precipitation. However, there are only trace amounts of nitrogen gas in the Martian atmosphere (Nier et al. 2003) and hence, it is unclear how Martian endolithic lichens would obtain their nitrogen supply. One possibility is that cyanobacteria in the rocks can fix sufficient nitrogen from the trace levels available to supply small populations of endolithic lichens. The paper by Joseph et al. (2019) also reviews the evidence for the possible presence of cyanobacteria on Mars and these organisms, especially members of the genera Nostoc, Scytonema, Stigonema, and Gloeocapsa, also form lichens on Earth.
First, in simulated environments, desiccation-induced breakdown of cell integrity was observed which was more severe under space than Martian conditions (Brandt et al. 2015; 2016). Hence, the Martian environment may be too extreme to support typical Earth-like extremophiles.
Second, it is doubtful lichens could survive on rock surfaces where they could be subjected to the scouring effects of Martian dust storms which may reach speeds up to 30 m s-1. Third, the majority of Earth lichens contain eukaryotic green alga, most usually members of the genera Trebouxia, Myrmecia, Coccomyxa, and Trentepohlia, as the photobiont and there is little evidence for such alga on Mars. Such algae might be present adjacent to areas which occasionally fill with water and along 'water pathways' and have been observed to be covered by very thin green mats suggestive of soil algae (Krupa 2017).
Fourth, putative fungi have been observed on Mars, many resembling basiodiomycota 'puffballs' apparently emerging from the ground (Joseph 2016). Some images even purport to show evidence of spores both on the surface of the specimens and littering adjacent ground (Joseph et al. 2019). Nevertheless, the 'puff-balls' could represent geological structures exposed and then covered by dust and soil. In addition, the majority of lichen fungi on Earth are ascomycota and very few species incorporate members of the basidiomycota (Hale 1967). Fifth, the basal thallus does not appear to be present in the published images but may be endolithic.
Hence, although Earth lichens may tolerate some aspects of extraterrestrial environments for a period of time, there is the question of their long-term survival in such circumstances. Martian lichens may have evolved an environmental tolerance significantly beyond that of Earth lichens and live an extremophile life in which the organism is essentially in continuous 'suspended animation', with very low levels of physiological activity only possible very over short periods of time.
Assuming Earth-like lichens on Mars, the following theoretical predictions may be made. First, they are likely to be crustose rather possessing a foliose or fruticose life form and therefore, less likely to be removed from surfaces and most likely to be endolithic. Third, they are likely to be extremely slow growing spending much of their time in a dehydrated state. Fourth, if they can survive on the surface of rocks, they are likely to possess an 'inverted' thallus structure to protect the photobiont, be darkly pigmented, or exist as scattered areolae on a black prothallus, the later to maximize the absorption of heat (Armstrong 2017). Fifth, association with cyanobacteria to fix nitrogen would be essential and Martian lichens may therefore require three or more symbionts to survive.
However, if lichens resembling D. baeomyces are present on Mars, then they appear to be able to survive on rock surfaces and form spores contrary to the assertions above. This observation suggests first, effective spore dispersal by Martian winds and second, that lichenization commonly occurs on the surface of Mars, likely to be a hazardous process. This assumption further presupposes the presence of eukaryotic green alga resembling Coccomyxa as algal partner. Moreover, despite the extreme conditions, the lichens appear able to fix enough carbon for growth, stress resistance, and to enable reproductive podetia to be formed in some numbers.
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