Australia: The Land Where Time Began

A biography of the Australian continent 

Surface Microbial Communities in the hyperarid Core of the Atacama Desert

There have been a number of rain events over the last 3 years that are highly unusual in the hyperarid core of the Atacama Desert, the driest and oldest desert on Earth, and this has resulted in the formation of hypersaline lagoons that have previously not been recorded, which lasted for several months. This study has analysed systematically the evolution of these lagoons in order to provide quantitative field constraints of large-scale impacts of the rain on the local microbial communities.  In this paper Azua-Bustos et al. show that the sudden mass input of water in regions that have been hyperarid for millions of years causes harm to most of the microbial species in the surface soil, which are adapted exquisitely adapted under conditions of very low amounts of liquid water, and succumb quickly by osmotic shock when water is suddenly abundantly available. Only a small number of bacteria, remarkably a newly identified species of Holomonas, remained metabolically active and had retained the ability to reproduce in the lagoons, though no eukaryotes or archaea were identified in these lagoons.  It is shown by this study that the biodiversity of microbial species, that was already low in extreme arid regions, diminished greatly when water is supplied rapidly and in large volumes. In conclusion, they placed their findings in the context of the astrobiological exploration of Mars, which is a hyperarid planet that in ancient times experienced catastrophic flooding.

Located in northern Chile, the Atacama Desert encompasses about 105,000 km². On the east it is bounded the Andes Mountains and on the west by the coastal Range. The hyperarid core of the Atacama (here “core Atacama”) has been arid for the past 15 Myr (Navarro-González et al., 2003; McKay et al., 2003; Hartley et al., 2005; Rech et al., 2006; Azua-Bustos et al., 2018). In the core Atacama mean annual precipitation is extremely low, with mean annual values that are mostly below 4 mm/m². As a result of the extreme aridity, the Yungay region, which is located in the core Atacama, was proposed in 2003 as a good analogue model for studies of Mars, and following more than 300 reports have detailed the meteorological, geophysical and biological characteristics of the core Atacama (Azua-Bustos et al., 2012). The soils of the core Atacama are highly saline, rich in nitrates, sulphates and perchlorates (Berger & Cooke, 1997; Böhlke et al., 1997; Ewing et al., 2007), and extremely poor in organics (Navarro-González et al., 2003; Azua-Bustos et al., 2015; Glavin et al., 2004; Buch, 2006). Though a number of microbial species from 3 domains of life have been reported as inhabiting the hyperarid core Atacama; these species are known as dry-tolerant and radiation-tolerant strains that also present elsewhere in the world, and they are exquisitely adapted to the extreme desiccating conditions, the high salinity ad the high UV radiation (Azua-Bustos et al., 2015; Azua-Bustos et al., 2012; Wierzchos et al., 2006; Paulino-Lima et al., 2013; Paulino-Lima et al., 2016) that have been present in the core Atacama for the past 150 Myr (Hartley et al., 2005).

In spite of its extreme dryness, parts of the Atacama Desert is often affected by the “altiplanic winter” between December and March, when moist moves from the east over the Andes Mountains which cause unsettled weather and occasional snow, mostly on the foothills of the Andes at the eastern edge of the core Atacama (Escobar et al., 2015). Over the past 3 years, exceptionally, most of the core Atacama has been impacted by 2 unique meteorological events: in 2015, 2 significant rain events were recorded on 25 March and 9 August; and in 2017 another was recorded on 7 June. The rain events that occurred in 2015 and 2017 originated as an extensive mass of clouds entered the core Atacama from the Pacific Ocean (from the west) during the last days of autumn, which was an unprecedented phenomenon occurred twice in only 3 years (Direcciόn Meteorolόgica de Chile, Climate Yearbooks). Mean annual precipitation reached values 1 order of magnitude higher than is usual for the region, up to 40 mm/m², which included other minor rain events in-between. It is suggested by climate models that similar rain events could occur about once every century, though there are no records of similar rain events for at least the last 500 years (Direcciόn Meteorolόgica de Chile, Climate Yearbooks; Bozkurt et al., 2016).

This significant alteration in weather patterns has been attributed to global climate change, with important shifts in rain patterns that have affected randomly different areas of the core Atacama (Fundaciόn, 2018), and though there are consequences that are not known on the composition, physiology and activity of the microbial species affected that are highly adapted to desiccation. The visual effect of these unusual rain events, that are most notable, has been the ponding of small lagoons that has never been documented previously in the Yungay region. Azua-Bustos et al. sampled 3 lagoons in Yungay 5 months after the 7 June 2017 rain event to assess quantitatively their characteristics that are volume-dependent and habitability in the long term.

Discussion and conclusions

The ecological equilibrium of the core Atacama altered by unprecedented flooding. Between 97% and 87% of the species that had been reported previously vanished from the soils of Yungay, only up to 4 species of bacteria surviving, 2 of which were in the most extreme case, in these new, though transitory water bodies. The results of this study of multiple combined geochemical and microbiological analyses of the lagoons that were newly formed in the hyperarid core of the Atacama Desert allowed Azua-Bustos et al. to propose the hypothesis that a massive and sudden water input in regions that had remained extremely arid for millions of years might cause most of the microbiological communities present in the surface soils to be disrupted. It was suggested by Azua-Bustos et al. that microbial species that had adapted exquisitely with very small amounts of water (Azua-Bustos et al., 2012) perished rapidly from osmotic shock following the flooding. In soil deeper than 15-20 cm below the surface the microbial communities would be likely to remain unaffected, as they live outside the upper layer that was analysed in this study.

Azua-Bustos et al. noted that it is possible that ecological recovery could occur after the lagoons were desiccated. The few bacterial groups that dominated 5 months after the rain event could reflect the fact that these groups were well adapted, or were faster growing, outcompeting the archaea and eukaryotes that may be present after the recovery sequence. Given that there are archaea or eukaryotes that are well adapted to this mid-range saline environment (Azua-Bustos et al., 2010), e.g. Dunaliella, it is possible that the initial population following the flood is growing up from the residential soil and salt-dome endolith populations. Azua-Bustos et al. suggested that colonisation by new microbial types that would be suitable to the new environment could presumably come later and, over time, there will be an increase in the complexity of the flood waters and soils as a result of incoming species. Azua-Bustos et al. were sampling surface and shallow subsurface soils, both wetted and submerged in water, monitoring the microbial diversity of the shallow flood waters over time, as well as analysing the timepoints since the rain events, in order to strengthen their conclusions further.

The core Atacama is a valid analogue for the N cycle and astrobiological studies on Mars. The operational definition of the “core Atacama” that is most useful is the distribution of nitrate deposits. The 13My. nitrate deposits (Rech et al.,2003) are what led the pioneering researchers to think there was a hyperarid core in the Atacama Desert, and as such, the Yungay site was chosen to be investigated because it was a near-historic nitrate deposit (Erickson, 1983). Nitrates appear to have been moved by fluvial action in these extremely old, dry and purportedly inactive surfaces, and yet they are present only in the core Atacama (Erickson, 1983), deposition in standing water is indicated by roughly equally potential surfaces that are present mostly at the bottom of valleys (Reich & Bao, 2018). Previous suggestions (Ewing et al., 2007) are supported by the geochemical analyses in this study that long periods of dryness build up nitrate deposits uniformly in the core Atacama, which accumulates atmospheric NO₃^-; it is further suggested by the results of this study that rare floods, such as those that have been reported for the first time in this paper, wash nitrates down to the floors of the valleys after which the water evaporates before the microbial denitrifiers have a chance to deplete the nitrate. It has been observed that high concentrations of nitrate inhibit denitrification: the nitrate gets higher as the water evaporates, biology cannot consume nitrate, so nitrification shuts down, and the nitrate deposits are formed. Fixed nitrogen has similarly been detected in sediments on Mars in the form of nitrates (Stern et al., 2015); however, it is still not clear whether a primitive nitrogen cycle ever developed on Mars, as the post-depositional behaviour of nitrates and the processes that are capable of recycling oxidised N back into the atmosphere are not known.

The results of this study in the core Atacama have provided the first coherent analogue for an incomplete N cycle on Mars: the formation of nitrate deposits being triggered by extreme dryness, which is punctuated by extreme flooding, which concentrates the nitrates in areas that are low-lying, and finally the floodwater evaporates before the nitrate can be consumed.

It is also suggested by the results obtained by Azua-Bustos et al. in this study from the Atacama Desert that there is a possible path for microbiological evolution on early Mars. Mars underwent a complex history of global climate change (Golombek et al., 2006), which included a first period between 4.5 and 3.5 Ga when there was an active surface hydrosphere, subsequently transitioning to increasingly desiccated conditions, and ultimately forming the vast dry desert of the Martian surface of the present. This transition was, however, episodically interrupted by enormous aqueous discharges the flooded regions of the surface on several occasions after 3.5 Ga, and carved what are the most voluminous channels in the solar System (Rodriguez et al., 2015). Consequently, hypothetical local ecosystems existing in some places on Mars, and adapted to the surface and subsurface of Mars that was increasingly dry after 3.5 Ga (Fairén et al., 2010), would have been episodically exposed later to osmotic stresses that were even stronger than those which have been reported in this paper for the microorganisms of the Atacama Desert. A consequence of this, after the earliest times the recurrence of liquid water on the surface of Mars might have contributed to the decimation of local or regional ecosystems, rather than being an opportunity for life to bloom again in the areas that had been flooded, and this would have contributed to a heterogeneous distribution of patchy inhabited habitats (Westall et al., 2013) during the history of Mars. Also, the negative results that were obtained by the instruments for detecting life onboard the Viking landers in 1976 (Brown et al., 1978) may find the simplest explanation in the fact that the samples in both the Gas Exchange and Labelled release experiments were incubated with various watery solutions (Klein, 1978) with high water activities. Any potential Martian cells in the samples would have been last exposed to such elevated water activity levels millions of years earlier, so their sampling and inclusion in the Viking experiments would have first caused them to burst by osmotic stress, and then the organic molecules due to the effect of the highly oxidant species that are characteristic of the Martian regolith (Hecht et al., 2009).

Sources & Further reading

1. Azua-Bustos, A., et al. (2018). "Unprecedented rains decimate surface microbial communities in the hyperarid core of the Atacama Desert." Scientific Reports 8(1): 16706.