Biosignatures and microbial fossils in endolithic microbial communities colonizing Ca-sulfate crusts in the Atacama Desert

Over the past 150 million years, the hyperarid core of the Atacama Desert has been transformed by geologic and atmospheric conditions into one of the most unique and inhospitable landscapes on the planet. This makes it an ideal Mars analog that has been explored for decades as preliminary studies on the space life discovery. However, two heavy rainfalls that occurred in the Atacama in 2015 and 2017 provide a unique opportunity to study the response of resident extremophiles to rapid environmental change associated with excessive water and salt shock. Here we combine geochemical analyses with molecular biology to study the variations in salts and microbial communities along an aridity gradient, and to examine the reshuffling of hyperarid microbiomes before and after the two rainfall events. Analysis of microbial community composition revealed that soils within the southern desert were consistently dominated by Actinobacteria, Proteobacteria, Acidobacteria, Planctomycetes, Chloroflexi, Bacteroidetes, Gemmatimonadetes, and Verrucomicrobia; soils within the hyperarid sites were dominated by Aquificae and Deinococcus-Thermus before heavy rainfalls, while these organisms almost totally diminished after rainfall, and the hyperarid microbial consortia and metabolisms transformed to a more southern desert pattern along with increased biodiversity. Salts at the shallow subsurface were dissolved and leached down to a deeper layer, both benefitting and challenging indigenous microorganisms with the excessive input of water and ions. Microbial viability was found to change with aridity and rainfall events but correlated with elevation, pH, conductivity, chloride, nitrate, sulfate, and soil organic matters (SOM). Metagenomic functional pathways related to stressor responses also increased in post-rainfall hyperarid soils. Our findings contribute to the primary goal of Atacama Mars analog research for understanding the microbial community structure and adaptations: this study sheds light on the structure of xerophilic, halophilic, and radioresistant microbiomes in hyperarid environments, and their response to changes in water availability.

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Fine scale diversification of endolithic microbial communities in the hyper-arid Atacama Desert

10.1101/218446 ◽

2017 ◽

Author(s):

Victoria Meslier ◽

Maria Cristina Casero ◽

Micah Dailey ◽

Jacek Wierzchos ◽

Carmen Ascaso ◽

...

Keyword(s):

Microbial Communities ◽

Water Retention ◽

High Throughput Sequencing ◽

Arid Zone ◽

Global Climate ◽

Atacama Desert ◽

Sampling Strategy ◽

Physical Structure ◽

Community Diversity ◽

Fine Scale

ABSTRACTThe expansion of desertification across our planet is accelerating as the result of human activity and global climate change. In hyper-arid deserts, endolithic microbial communities colonize the rocks’ interior as a survival strategy. Yet, the composition of these communities and the drivers promoting their assembly are still poorly understood. Using a sampling strategy that minimized climate regime and biogeography effects, we analyzed the diversity and community composition of endoliths from four different lithic substrates – calcite, gypsum, ignimbrite and granite – collected in the hyper-arid zone of the Atacama Desert, Chile. By combining microscopy, mineralogy, and high throughput sequencing, we found these communities to be highly specific to their lithic substrate, although they were all dominated by the same four main phyla, Cyanobacteria, Actinobacteria, Chloroflexi and Proteobacteria. This finding indicates a fine scale diversification of the microbial reservoir driven by substrate properties. Our data suggest that the overall rock chemistry is not an essential driver of community structure and we propose that the architecture of the rock, i.e. the space available for colonization and its physical structure, linked to water retention capabilities, is ultimately the driver of community diversity and composition at the dry limit of life.Originality-Significance StatementIn this study, we demonstrated that endolithic microbial communities are highly specific to their substrates, suggesting a fine scale diversification of the available microbial reservoir. By using an array of rock substrates from the same climatic region, we established, for the first time, that the architecture of the rock is linked to water retention and is ultimately the driver of community diversity and composition at the dry limit for life.

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Author Correction: Unprecedented rains decimate surface microbial communities in the hyperarid core of the Atacama Desert

Scientific Reports ◽

10.1038/s41598-019-40319-w ◽

2019 ◽

Vol 9 (1) ◽

Author(s):

A. Azua-Bustos ◽

A. G. Fairén ◽

C. González-Silva ◽

C. Ascaso ◽

D. Carrizo ◽

...

Keyword(s):

Microbial Communities ◽

Atacama Desert

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In situ metabolism in halite endolithic microbial communities of the hyperarid Atacama Desert

Frontiers in Microbiology ◽

10.3389/fmicb.2015.01035 ◽

2015 ◽

Vol 6 ◽

Cited By ~ 22

Author(s):

Alfonso F. Davila ◽

Ian Hawes ◽

Jonathan G. Araya ◽

Diego R. Gelsinger ◽

Jocelyne DiRuggiero ◽

...

Keyword(s):

Microbial Communities ◽

Atacama Desert

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Radiocarbon Evidence of Active Endolithic Microbial Communities in the Hyperarid Core of the Atacama Desert

Astrobiology ◽

10.1089/ast.2012.0854 ◽

2013 ◽

Vol 13 (7) ◽

pp. 607-616 ◽

Cited By ~ 32

Author(s):

Lori A. Ziolkowski ◽

Jacek Wierzchos ◽

Alfonso F. Davila ◽

Gregory F. Slater

Keyword(s):

Microbial Communities ◽

Atacama Desert

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Distribution of scytonemin in endolithic microbial communities from halite crusts in the hyperarid zone of the Atacama Desert, Chile

FEMS Microbiology Ecology ◽

10.1111/1574-6941.12387 ◽

2014 ◽

pp. n/a-n/a ◽

Cited By ~ 14

Author(s):

Petr Vítek ◽

Jan Jehlička ◽

Carmen Ascaso ◽

Vlastimil Mašek ◽

Benito Gómez-Silva ◽

...

Keyword(s):

Microbial Communities ◽

Atacama Desert

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Spatial Variability of Microbial Communities and Salt Distributions Across a Latitudinal Aridity Gradient in the Atacama Desert

Microbial Ecology ◽

10.1007/s00248-020-01672-w ◽

2021 ◽

Author(s):

Jianxun Shen ◽

Adam J. Wyness ◽

Mark W. Claire ◽

Aubrey L. Zerkle

Keyword(s):

Microbial Communities ◽

Microbial Community Composition ◽

Atacama Desert ◽

Microbial Consortia ◽

Event Analysis ◽

Rainfall Events ◽

Aridity Gradient ◽

Shallow Subsurface ◽

Salt Shock ◽

Arid Desert

AbstractOver the past 150 million years, the Chilean Atacama Desert has been transformed into one of the most inhospitable landscapes by geophysical changes, which makes it an ideal Mars analog that has been explored for decades. However, a heavy rainfall that occurred in the Atacama in 2017 provides a unique opportunity to study the response of resident extremophiles to rapid environmental change associated with excessive water and salt shock. Here we combine mineral/salt composition measurements, amendment cell culture experiments, and next-generation sequencing analyses to study the variations in salts and microbial communities along a latitudinal aridity gradient of the Atacama Desert. In addition, we examine the reshuffling of Atacama microbiomes after the rainfall event. Analysis of microbial community composition revealed that soils within the southern arid desert were consistently dominated by Actinobacteria, Chloroflexi, Proteobacteria, Firmicutes, Bacteroidetes, Gemmatimonadetes, Planctomycetes, and Acidobacteria, and Verrucomicrobia. Intriguingly, the hyperarid microbial consortia exhibited a similar pattern to the more southern desert. Salts at the shallow subsurface were dissolved and leached down to a deeper layer, challenging indigenous microorganisms with the increasing osmotic stress. Microbial viability was found to change with aridity and rainfall events. This study sheds light on the structure of xerotolerant, halotolerant, and radioresistant microbiomes from the hyperarid northern desert to the less arid southern transition region, as well as their response to changes in water availability.

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The composition of endolithic communities in gypcrete is determined by the specific microhabitat architecture

10.5194/bg-2020-245 ◽

2020 ◽

Author(s):

María Cristina Casero ◽

Victoria Meslier ◽

Jocelyne DiRuggiero ◽

Antonio Quesada ◽

Carmen Ascaso ◽

...

Keyword(s):

Microbial Communities ◽

High Throughput ◽

Environmental Conditions ◽

High Throughput Sequencing ◽

Atacama Desert ◽

Bottom Layer ◽

Essential Factor ◽

Microscopy Techniques ◽

First Time ◽

Endolithic Communities

Abstract. Endolithic microhabitats have been described as the last refuge for life in arid and hyper-arid deserts where life has to deal with harsh environmental conditions. A number of rock substrates from the hyper-arid Atacama Desert, colonized by endolithic microbial communities, such as halite, gypsum crusts, gypcrete, calcite, granite and ignimbrite, have been characterized and compared using different approaches. In this work, three different endolithic microhabitats are described, each one with a particular origin and architecture, found within a lithic substrate known as gypcrete. Gypcrete, an evaporitic rock mainly composed of gypsum (CaSO4 ⋅ 2H2O) and collected in the Cordón de Lila area of the desert (Preandean Atacama Desert), was found to harbour cryptoendolithic (within pore spaces in the rock), chasmoendolithic (within cracks and fissures) and hypoendolithic (within microcave-like pores in rock-bottom layer) microhabitats. A combination of microscopy investigations strategies and high-throughput sequencing approaches were used to characterize the endolithic communities at the microscale in these microhabitats within the same piece of lithic substrate. Microscopy techniques revealed differences in the architecture of the endolithic microhabitats and in the distribution of the microorganisms within those microhabitats. Cyanobacteria and Proteobacteria were dominant in the endolithic communities, of which the hypoendolithic community was the least diverse and hosted unique taxa. These results show, for the first time, that the differences in the architecture of a microhabitat, even within the same piece of lithic substrate, might be an essential factor in shaping the diversity and composition of endolithic microbial communities.

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