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Title: Microbial Community Structure and the Persistence of Cyanobacterial Populations in Salt Crusts of the Hyperarid Atacama Desert from Genome-Resolved Metagenomics

Abstract

Although once thought to be devoid of biology, recent studies have identified salt deposits as oases for life in the hyperarid Atacama Desert. To examine spatial patterns of microbial species and key nutrient sources, we genomically characterized 26 salt crusts from three sites along a fog gradient. The communities are dominated by a large variety of Halobacteriales and Bacteroidetes, plus a few algal and Cyanobacterial species. CRISPR locus analysis suggests the distribution of a single Cyanobacterial population among all sites. This is in stark contrast to the extremely high sample specificity of most other community members. Only present at the highest moisture site is a genomically characterized Thermoplasmatales archaeon (Marine Group II) and six Nanohaloarchaea, one of which is represented by a complete genome. Parcubacteria (OD1) and Saccharibacteria (TM7), not previously reported from hypersaline environments, were found at low abundances. We found no indication of a N2 fixation pathway in the communities, suggesting acquisition of bioavailable nitrogen from atmospherically derived nitrate. Samples cluster by site based on bacterial and archaeal abundance patterns and photosynthetic capacity decreases with increasing distance from the ocean. We conclude that moisture level, controlled by coastal fog intensity, is the strongest driver of community membership.

Authors:
 [1];  [2];  [2];  [3];  [4];  [4];  [1];  [5]
  1. Univ. of California, Berkeley, CA (United States). Department of Environmental Science, Policy, and Management
  2. Univ. of California, Berkeley, CA (United States). Department of Earth and Planetary Sciences
  3. Univ. of California, Berkeley, CA (United States). Department of Environmental Science, Policy, and Management; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Ecology Department, Earth Sciences Division
  4. Universidad Catolica del Norte, Antofagasta (Chile). Centro de Biotecnologia
  5. Univ. of California, Berkeley, CA (United States). Department of Environmental Science, Policy, and Management and Department of Earth and Planetary Sciences
Publication Date:
Research Org.:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1393344
Alternate Identifier(s):
OSTI ID: 1408450
Report Number(s):
LLNL-JRNL-706877
Journal ID: ISSN 1664-302X
Grant/Contract Number:  
AC52-07NA27344; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; metagenome; Atacama Desert; salt crust; hyperarid; hypersaline; environmental genomics; salar

Citation Formats

Finstad, Kari M., Probst, Alexander J., Thomas, Brian C., Andersen, Gary L., Demergasso, Cecilia, Echeverría, Alex, Amundson, Ronald G., and Banfield, Jillian F. Microbial Community Structure and the Persistence of Cyanobacterial Populations in Salt Crusts of the Hyperarid Atacama Desert from Genome-Resolved Metagenomics. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.01435.
Finstad, Kari M., Probst, Alexander J., Thomas, Brian C., Andersen, Gary L., Demergasso, Cecilia, Echeverría, Alex, Amundson, Ronald G., & Banfield, Jillian F. Microbial Community Structure and the Persistence of Cyanobacterial Populations in Salt Crusts of the Hyperarid Atacama Desert from Genome-Resolved Metagenomics. United States. https://doi.org/10.3389/fmicb.2017.01435
Finstad, Kari M., Probst, Alexander J., Thomas, Brian C., Andersen, Gary L., Demergasso, Cecilia, Echeverría, Alex, Amundson, Ronald G., and Banfield, Jillian F. Fri . "Microbial Community Structure and the Persistence of Cyanobacterial Populations in Salt Crusts of the Hyperarid Atacama Desert from Genome-Resolved Metagenomics". United States. https://doi.org/10.3389/fmicb.2017.01435. https://www.osti.gov/servlets/purl/1393344.
@article{osti_1393344,
title = {Microbial Community Structure and the Persistence of Cyanobacterial Populations in Salt Crusts of the Hyperarid Atacama Desert from Genome-Resolved Metagenomics},
author = {Finstad, Kari M. and Probst, Alexander J. and Thomas, Brian C. and Andersen, Gary L. and Demergasso, Cecilia and Echeverría, Alex and Amundson, Ronald G. and Banfield, Jillian F.},
abstractNote = {Although once thought to be devoid of biology, recent studies have identified salt deposits as oases for life in the hyperarid Atacama Desert. To examine spatial patterns of microbial species and key nutrient sources, we genomically characterized 26 salt crusts from three sites along a fog gradient. The communities are dominated by a large variety of Halobacteriales and Bacteroidetes, plus a few algal and Cyanobacterial species. CRISPR locus analysis suggests the distribution of a single Cyanobacterial population among all sites. This is in stark contrast to the extremely high sample specificity of most other community members. Only present at the highest moisture site is a genomically characterized Thermoplasmatales archaeon (Marine Group II) and six Nanohaloarchaea, one of which is represented by a complete genome. Parcubacteria (OD1) and Saccharibacteria (TM7), not previously reported from hypersaline environments, were found at low abundances. We found no indication of a N2 fixation pathway in the communities, suggesting acquisition of bioavailable nitrogen from atmospherically derived nitrate. Samples cluster by site based on bacterial and archaeal abundance patterns and photosynthetic capacity decreases with increasing distance from the ocean. We conclude that moisture level, controlled by coastal fog intensity, is the strongest driver of community membership.},
doi = {10.3389/fmicb.2017.01435},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {Fri Jul 28 00:00:00 EDT 2017},
month = {Fri Jul 28 00:00:00 EDT 2017}
}

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Microbial life at high salt concentrations: phylogenetic and metabolic diversity
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Deep-Sea Oil Plume Enriches Indigenous Oil-Degrading Bacteria
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High-Density Universal 16S rRNA Microarray Analysis Reveals Broader Diversity than Typical Clone Library When Sampling the Environment
journal, March 2007


Cyanobacteria in hypersaline environments: biodiversity and physiological properties
journal, March 2015


Microbial Colonization of the Salt Deposits in the Driest Place of the Atacama Desert (Chile)
journal, June 2012

  • Stivaletta, Nunzia; Barbieri, Roberto; Billi, Daniela
  • Origins of Life and Evolution of Biospheres, Vol. 42, Issue 2-3
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Binning Metagenomic Contigs Using Unsupervised Clustering and Reference Databases
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Long term atmospheric deposition as the source of nitrate and other salts in the Atacama Desert, Chile: New evidence from mass-independent oxygen isotopic compositions
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  • Geochimica et Cosmochimica Acta, Vol. 68, Issue 20
  • DOI: 10.1016/j.gca.2004.04.009

Rates and geochemical processes of soil and salt crust formation in Salars of the Atacama Desert, Chile
journal, December 2016


Life in extreme environments
journal, February 2001

  • Rothschild, Lynn J.; Mancinelli, Rocco L.
  • Nature, Vol. 409, Issue 6823
  • DOI: 10.1038/35059215

A new view of the tree of life
journal, April 2016


Neogene evaporites in desert volcanic environments: Atacama Desert, northern Chile: Neogene evaporites in desert volcanic environments
journal, December 2001


Urban aerosols harbor diverse and dynamic bacterial populations
journal, December 2006

  • Brodie, E. L.; DeSantis, T. Z.; Parker, J. P. M.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 1, p. 299-304
  • DOI: 10.1073/pnas.0608255104

Endolithic Cyanobacteria in Halite Rocks from the Hyperarid Core of the Atacama Desert
journal, June 2006

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Search and clustering orders of magnitude faster than BLAST
journal, August 2010


IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats
journal, May 2007

  • Grissa, I.; Vergnaud, G.; Pourcel, C.
  • Nucleic Acids Research, Vol. 35, Issue Web Server
  • DOI: 10.1093/nar/gkm360

Hypolithic community shifts occur as a result of liquid water availability along environmental gradients in China's hot and cold hyperarid deserts
journal, February 2007


The ecology of the extremely halophilic archaea
journal, April 1994


Mars-Like Soils in the Atacama Desert, Chile, and the Dry Limit of Microbial Life
journal, November 2003


Deep-Sea Oil Plume Enriches Indigenous Oil-Degrading Bacteria
journal, August 2010


Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla
journal, September 2012


Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


Microbial life at high salt concentrations: phylogenetic and metabolic diversity
journal, January 2008


A viability-linked metagenomic analysis of cleanroom environments: eukarya, prokaryotes, and viruses
journal, December 2015


Works referencing / citing this record:

Active microbiome structure and its association with environmental factors and viruses at different aquatic sites of a high‐altitude wetland
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Halophilic microbial community compositional shift after a rare rainfall in the Atacama Desert
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Transitory microbial habitat in the hyperarid Atacama Desert
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Fundamental drivers for endolithic microbial community assemblies in the hyperarid Atacama Desert: Desert Endolithic Microbial Communities
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Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community
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Rare calcium chloride–rich soil and implications for the existence of liquid water in a hyperarid environment
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Living at the Frontiers of Life: Extremophiles in Chile and Their Potential for Bioremediation
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Applying Genome-Resolved Metagenomics to Deconvolute the Halophilic Microbiome
journal, March 2019


Metagenomics of Atacama Lithobiontic Extremophile Life Unveils Highlights on Fungal Communities, Biogeochemical Cycles and Carbohydrate-Active Enzymes
journal, November 2019


Cellular life from the three domains and viruses are transcriptionally active in a hypersaline desert community
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Transitory microbial habitat in the hyperarid Atacama Desert
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Living at the Frontiers of Life: Extremophiles in Chile and Their Potential for Bioremediation
journal, October 2018

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  • Frontiers in Microbiology, Vol. 9
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Applying Genome-Resolved Metagenomics to Deconvolute the Halophilic Microbiome
journal, March 2019


Metagenomics of Atacama Lithobiontic Extremophile Life Unveils Highlights on Fungal Communities, Biogeochemical Cycles and Carbohydrate-Active Enzymes
journal, November 2019