- Proceedings of the National Academy of Sciences of the United States of America
- Published 6 months ago
Traces of life are nearly ubiquitous on Earth. However, a central unresolved question is whether these traces always indicate an active microbial community or whether, in extreme environments, such as hyperarid deserts, they instead reflect just dormant or dead cells. Although microbial biomass and diversity decrease with increasing aridity in the Atacama Desert, we provide multiple lines of evidence for the presence of an at times metabolically active, microbial community in one of the driest places on Earth. We base this observation on four major lines of evidence: (i) a physico-chemical characterization of the soil habitability after an exceptional rain event, (ii) identified biomolecules indicative of potentially active cells [e.g., presence of ATP, phospholipid fatty acids (PLFAs), metabolites, and enzymatic activity], (iii) measurements of in situ replication rates of genomes of uncultivated bacteria reconstructed from selected samples, and (iv) microbial community patterns specific to soil parameters and depths. We infer that the microbial populations have undergone selection and adaptation in response to their specific soil microenvironment and in particular to the degree of aridity. Collectively, our results highlight that even the hyperarid Atacama Desert can provide a habitable environment for microorganisms that allows them to become metabolically active following an episodic increase in moisture and that once it decreases, so does the activity of the microbiota. These results have implications for the prospect of life on other planets such as Mars, which has transitioned from an earlier wetter environment to today’s extreme hyperaridity.
We have recently discovered a variety of unrelated phototrophic microorganisms (two microalgae and one cyanobacteria) in specialized terrestrial habitats at The Coastal Range of the Atacama Desert. Interestingly, morphological and molecular evidence suggest that these three species are all recent colonists that came from aquatic habitats. The first case is Cyanidiales inhabiting coastal caves. Cyanidiales are microalgae that are commonly found in warm acid springs, but have also been recently discovered as cave flora in Italy. The case is Dunaliella biofilms colonizing spider webs in coastal caves; Dunaliella are microalgae typically found in hypersaline habitats. The third case is Chroococcidiopsis, a genus of Cyanobacteria commonly found in deserts around the world that has also been described in warm springs. Thus, we show that the traits found in the closest ancestors of the aforementioned species (which inhabited other unrelated extreme environments) seem to be now useful for the described species in their current subaerial habitats and may likely correspond to cases of exaptations. Altogether, the Coastal Range of the Atacama Desert may be considered as a place where key steps on the colonization of land by phototrophic organisms seem to be being repeated by convergent evolution of extant microalgae and Cyanobacteria.
The Atacama Desert has been pointed out as one of the places on earth where the highest surface irradiance may occur. This area is characterized by its high altitude, prevalent cloudless conditions and relatively low columns of ozone and water vapor. Aimed at the characterization of the solar spectrum in the Atacama Desert, we carried out in February-March 2015 ground-based measurements of the spectral irradiance (from the ultraviolet to the near infrared) at seven locations that ranged from the city of Antofagasta (on the southern pacific coastline) to the Chajnantor Plateau (5,100 m altitude). Our spectral measurements allowed us to retrieve the total ozone column, the precipitable water, and the aerosol properties at each location. We found that changes in these parameters, as well as the shorter optical path length at high-altitude locations, lead to significant increases in the surface irradiance with the altitude. Our measurements show that, in the range 0-5100 m altitude, surface irradiance increases with the altitude by about 27% in the infrared range, 6% in the visible range, and 20% in the ultraviolet range. Spectral measurements carried out at the Izaña Observatory (Tenerife, Spain), in Hannover (Germany) and in Santiago (Chile), were used for further comparisons.
The Atacama Desert is the most extreme non-polar biome on Earth, the core region of which is considered to represent the dry limit for life and to be an analogue for Martian soils. This study focused on actinobacteria because they are keystone species in terrestrial ecosystems and are acknowledged as an unrivalled source of bioactive compounds. Metagenomic analyses of hyper-arid and extreme hyper-arid soils in this desert revealed a remarkable degree of actinobacterial ‘dark matter’, evidenced by a detected increase of 34% in families against those that are validly published. Rank-abundance analyses indicated that these soils were high-diversity habitats and that the great majority of designated ‘rare’ genera (up to 60% of all phylotypes) were always rare. These studies have enabled a core actinobacterial microbiome common to both habitats to be defined. The great majority of detected taxa have not been recovered by culture dependent methods, neither, with very few exceptions, has their functional ecology been explored. A microbial seed bank of this magnitude has significance not just for Atacama soil ecosystem resilience but represents an enormous untapped resource for biotechnology discovery programmes in an era where resistance to existing antibiotics is rapidly becoming a major threat to global health.
Archaeological and palaeoecological studies throughout the Americas have documented widespread landscape and environmental transformation during the pre-Columbian era. The highly dynamic Formative (or Neolithic) period in northern Chile (ca. 3700-1550 yr BP) brought about the local establishment of agriculture, introduction of new crops (maize, quinoa, manioc, beans, etc.) along with a major population increase, new emergent villages and technological innovations. Even trees such as the Algarrobos (Prosopis section Algarobia) may have been part of this transformation. Here, we provide evidence that these species were not native to the Atacama Desert of Chile (18-27°S), appearing only in the late Holocene and most likely due to human actions. We assembled a database composed of 41 taxon specific AMS radiocarbon dates from archaeobotanical and palaeoecological records (rodent middens, leaf litter deposits), as well an extensive bibliographical review comprising archaeobotanical, paleoecological, phylogenetic and taxonomic data to evaluate the chronology of introduction and dispersal of these trees. Although Algarrobos could have appeared as early as 4200 yr BP in northernmost Chile, they only became common throughout the Atacama over a thousand years later, during and after the Formative period. Cultural and natural factors likely contributed to its spread and consolidation as a major silvicultural resource.
This study reports data on arsenic speciation in two green algae species (Cladophora sp. and Chara sp.) and in five aquatic plants (Azolla sp., Myriophyllum aquaticum, Phylloscirpus cf. desserticola, Potamogeton pectinatus, Ruppia filifolia and Zannichellia palustris) from the Loa River Basin in the Atacama Desert (northern Chile). Arsenic content was measured by Mass spectrometry coupled with Inductively Coupled Plasma (ICP-MS), after acidic digestion. Liquid chromatography coupled to ICP-MS was used for arsenic speciation, using both anionic and cationic chromatographic exchange systems. Inorganic arsenic compounds were the main arsenic species measured in all samples. The main arsenic species in the extracts of freshwater algae and plants were arsenite and arsenate, whereas glycerol-arsenosugar (gly-sug), dimethylarsinic acid (DMA) and methylarsonic acid (MA) were present only as minor constituents. Of the samples studied, algae species accumulated more arsenic than aquatic plants. Total arsenic content ranged from 182 to 11100 and from 20 to 248mgAskg(-1) (d.w.) in algae and freshwater plants, respectively. In comparison with As concentration in water samples, there was hyper-accumulation (>0.1% d.w.) in Cladophora sp.
The C3 plant Rhazya stricta is native to arid desert environment zones, where it experiences daily extremes of heat, light intensity (PAR) and high vapour pressure deficit (VPD). We measured the photosynthetic parameters in R. stricta in its native environment to assess the mechanisms that permit it to survive in these extreme conditions. Infrared gas exchange analysis examined diel changes in assimilation (A), stomatal conductance (gs ) and transpiration (E) on mature leaves of R. stricta. A/ci analysis was used to determine the effect of temperature on carboxylation capacity (Vc,max ) and the light- and CO2 -saturated rate of photosynthesis (Amax ). Combined chlorophyll fluorescence and gas exchange light response curve analysis at ambient and low oxygen showed that both carboxylation and oxygenation of Rubisco acted as the major sinks for the end products of electron transport. Physiological analysis in conjunction with gene expression analysis suggested that there are two isoforms of Rubisco activase which may provide an explanation for the ability of R. stricta to maintain Rubisco function at high temperatures. The potential to exploit this ability to cope with extreme temperatures is discussed in the context of future crop improvement.
The Raman imaging method was successfully applied for mapping the distribution of biomolecules (e.g., pigments) associated with cryptoendolithic and hypoendolithic microorganisms, as well as the inorganic host mineral matrix that forms the habitat for the biota. To the best of our knowledge, this is the first comprehensive study in the field of geomicrobiology based on this technique. The studied microbial ecosystem was located nearly 3000 m above sea level within the driest desert on Earth, the Atacama in Chile. Enhancement of carotenoid Raman signal intensity close to the surface was registered at different areas of endolithic colonization dominated by algae, with cyanobacteria present as well. This is interpreted as an adaptation mechanism to the excessive solar irradiation. On the other hand, cyanobacteria synthesize scytonemin as a passive UV-screening pigment (found at both the hypoendolithic and cryptoendolithic positions). The distribution of the scytonemin Raman signal was mapped simultaneously with the surrounding mineral matrix. Thus, mapping was done of the phototrophic microorganisms in their original microhabitat together with the host rock environment. Important information which was resolved from the Raman imaging dataset of the host rock is about the hydration state of Ca-sulfate, demonstrated on the presence of gypsum (CaSO4·2H2O) and the absence of both anhydrite (CaSO4) and bassanite (CaSO4·1/2H2O). Obtaining combined “in situ” simultaneous information from the geological matrix (inorganic) together with the microbial biomolecules (organic) is discussed and concluded as an important advantage of this technique. We discuss how selection of the laser wavelength (785 and 514.5-nm) influences the Raman imaging results.
- Proceedings of the National Academy of Sciences of the United States of America
- Published over 5 years ago
For centuries ecologists have studied how the diversity and functional traits of plant and animal communities vary across biomes. In contrast, we have only just begun exploring similar questions for soil microbial communities despite soil microbes being the dominant engines of biogeochemical cycles and a major pool of living biomass in terrestrial ecosystems. We used metagenomic sequencing to compare the composition and functional attributes of 16 soil microbial communities collected from cold deserts, hot deserts, forests, grasslands, and tundra. Those communities found in plant-free cold desert soils typically had the lowest levels of functional diversity (diversity of protein-coding gene categories) and the lowest levels of phylogenetic and taxonomic diversity. Across all soils, functional beta diversity was strongly correlated with taxonomic and phylogenetic beta diversity; the desert microbial communities were clearly distinct from the nondesert communities regardless of the metric used. The desert communities had higher relative abundances of genes associated with osmoregulation and dormancy, but lower relative abundances of genes associated with nutrient cycling and the catabolism of plant-derived organic compounds. Antibiotic resistance genes were consistently threefold less abundant in the desert soils than in the nondesert soils, suggesting that abiotic conditions, not competitive interactions, are more important in shaping the desert microbial communities. As the most comprehensive survey of soil taxonomic, phylogenetic, and functional diversity to date, this study demonstrates that metagenomic approaches can be used to build a predictive understanding of how microbial diversity and function vary across terrestrial biomes.
Cataglyphis desert ants are impressive navigators. When the foragers roam the desert, they employ path integration. For these ants, distance estimation is one key challenge. Distance information was thought to be provided by optic flow (OF)-that is, image motion experienced during travel-but this idea was abandoned when stride integration was discovered as an odometer mechanism in ants. We show that ants transported by nest mates are capable of measuring travel distance exclusively by the use of OF cues. Furthermore, we demonstrate that the information gained from the optic flowmeter cannot be transferred to the stride integrator. Our results suggest a dual information channel that allows the ants to measure distances by strides and OF cues, although both systems operate independently and in a redundant manner.