Results above allow us to characterize the Puquios in terms of heterogeneity. Heterogeneity in turn may foster ecosystem resilience, enabling habitability within the polyextreme conditions that characterize the hyper arid environment of the Atacama Desert (sensu57).
Heterogeneity of biota, microbial communities, lagoon bottom types and type of mineral precipitation within the Puquios as documented above, appears to be driven by spatial variability in brine chemistry. Variations in water level and brine chemistry may drive changes in microbial communities as their abundances and functions respond to changing environmental conditions through time. Functional redundancy in the system is hypothesized to contribute to a high degree of resilience in response to changes in brine chemistry and lifestyle allowing these microbial communities to persist in harsh poly-extreme conditions. Where EC is relatively low, as in Puquio 1 and the Transition Zone, microbial mats are common (Supplemental Fig. S4a – S4c) and the microscopic analysis revealed a heterogeneous distribution of filamentous and unicellular cyanobacteria, cell morphologies compatible with chromatium and diatoms (Supplemental Fig. S5). Abundances of phytobenthos and zoobenthos are relatively high, and mineral deposition, primarily gypsum, is largely microbially driven. In contrast, when brines have high EC values, such as those observed in Puquio 2 (Fig. 2c, F, Supplemental Fig. S1) the occurrence of microbial mats is rare and the bottom is covered by gypsum crystals, water column biota are present in lower proportions, and gypsum precipitation appears to be largely physicochemical (Supplemental Fig. S4d). Although more work is needed to delineate physicochemical versus microbial controls on gypsum precipitation, mineral precipitation in Puquio 3 appears influenced by both microbial and physicochemical controls, whereas Puquio 4 appears dominated by physicochemical controls. In both sites microbial mats are covered by different gypsum morphologies (Supplemental Fig. S4e, S4f, respectively).
Heterogeneity observed in all studied aspects of the Puquios is hypothesized to generate a system that contains diverse ecological niches within the brines, porewaters, subaerial structures, and microbial mats that characterize this system. Furthermore, seasonal changes in brine chemistry and water level in the system, are likely to impact all of the ecological niches to varying degrees. Dynamic interplay between physical, chemical, geological and biological processes is thought to generate unique communities that foster different styles of life, including both the community structure and function. For example, the Invierno Altiplanico that occurred in January – February 2017 is hypothesized to have impacted both water levels and microbial communities in Puquio 1. Higher water levels after the Invierno Altiplanico likely filled the pore spaces of the subaerially exposed structures, reduced available oxygen in the environment that fosters endoevaporitic microbial communities, and produced the observed enrichment in the anaerobic microbial population in Puquio 1 samples during the March 2017 field campaign. The surface water level therefore is an important determinant of the shift from a subaerial to a subaqueous lifestyle as was previously observed58. Considering that EC has an indirect correlation with surface water level in the Puquios (R2 = 0.50 to 0.83), seasonally variable water levels in Puquio 1 may drive the relationship between EC and microbial community structure in Puquio 1, distinguishing it from similar endoevaporitic communities near Puquios 2, 3 and 4. Similar seasonal differences in Anaerobic Deltaproteobacteria abundances were observed between summer and winter samples in a previous study17 and between the depths analyzed in subaqueous niches in March 201229.
Gradients in environmental parameters have previously been described in the Puquios32,59,60, as well as in a variety of Andean microbial ecosystems, such as Lake Tebenquiche in Chile25, Lake La Brava in Chile, and Lake Socompa in Argentina19,23,27. These environmental settings are associated with biological communities that are tolerant to extreme conditions17, including a reduced group of invertebrates, such as brine shrimps, insects and other planktonic organisms, as well as macrophytes adjacent to the ponds61–65. Phototrophs in the desert lagoons are mainly represented by diatoms and cyanobacteria25,66,67, with broad representation of phototrophic microbial communities 68. Diatoms have been well-studied as a result of their abundance in all Northern Chile aquatic systems. Species in both groups function as indicators of water chemistry characteristics65.
Beyond Andean microbial ecosystems, extreme environments have been observed in other modern and ancient hypersaline lagoons, lakes in arid settings, sabkha environments, and anthropogenically-driven evaporite depositional settings, such as the salt works at Guerrero Negro69–71 and the EMISAL salt works in Egypt72,73. Such extreme conditions typically subject resident biota to wide fluctuations in temperature, salinity, pH, dissolved oxygen, total dissolved solids and redox potential74,75. In these environments, high light intensity is often coupled with low-redox potential and low oxygen concentration; heavy metals and nutrients may also fluctuate (sensu76). As such, observations of horizontal and vertical heterogeneity in brine chemistry, in particular electrical conductivity, and the corresponding diversity of the biological and mineralogical components of the Puquios appear to be characteristic of extreme environments. Similarly, shallow lagoons within these settings may be subject to long periods of desiccation during seasonal changes. Moreover, seasonal and interannual variability in climate, aridity, water activity, UV, and temperature will likely produce even more dramatic environmental gradients than those observed during the November 2017 field campaign.
Furthermore, ecosystem heterogeneity is an important driver of biodiversity and ecosystem resilience (e.g. 77–81), that would enable habitability within the polyextreme environmental conditions of the Puquios. Heterogeneity fosters resilience to environmental change as a result of multiple factors at various levels of biological organization79. At the landscape level, spatial heterogeneity affects localized responses to perturbations82, providing a greater range of resources and microenvironments that can act as buffers to inhabitants78,83−85. In the Puquios, spatial heterogeneity of brine chemistry is a dominant driver of microbial diversity and the dominant metabolic pathways between brine communities and E1 layer of the subaerial structures. Most notable was the diversity within the E1 layer communities given they reside above the brines and are largely phototrophic, yet they are impacted by the surrounding brines. The strong brine chemical gradient across the Puquio system provides juxtaposed habitats that can provide nutrients and resources to support heterotrophically dominated aqueous communities as well as halotolerant communities on the extreme end, and autotrophic communities in the subaerial structures. The overall diversity appears to be created by a geochemical architecture where mineral precipitation creates multiple niches where metabolically flexible communities can persist in a polyextreme environment. Indeed, studies have shown that community diversity increases the capacity of biota to survive and/or recover from perturbations (e.g. 86–88).
Spatial heterogeneity coupled with complexity promotes species coexistence by providing a wide range of niche environments, which can enhance species diversity89. Spatially variable brine chemistry in the Puquios was shown to generate a diversity of biological communities in both planktic and benthic communities of eukaryotes and prokaryotes, a gradient in the role of biological influence on mineral deposition, and a variety of mineral assemblages. These intra- and interspecific variations allow redundancy, combined functioning and interaction of species, as well as differing responses, tolerances, and adaptability (sensu79), which is critical for the ecosystem to thrive in response to environmental perturbations, leading to resilience at multiple scales.
On the scale of microns to hundreds of meters, these multi-disciplinary observations of the Puquios provide a case study of the inherent heterogeneity unique to these extreme environments. We argue that the importance of variability observed in the Puquios at multiple scales can likely be extended to encompass the wider complex of Andean microbial ecosystems in all of northern Chile, Argentina, and Bolivia8. Spanning several orders of magnitude, this spatial heterogeneity of physical, chemical, biological and geological processes observed is hypothesized to be the cornerstone for the resilience of these ecosystems that persist in some of the harshest conditions on Earth.