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  • Review Article
  • Published:

Xerotolerant bacteria: surviving through a dry spell

Nature Reviews Microbiology volume 15, pages 285–296 (2017)Cite this article

Subjects

Key Points

  • Xerotolerant microorganisms are extremophiles that can survive in environments with extremely limited water availability. Despite their importance to these ecosystems, xerotolerant bacteria have been largely overlooked.

  • A high diversity of xerotolerant bacteria can be found in many different extreme environments, including hot and cold environments, such as the Atacama and Antarctic deserts. In these biomes, xerotolerant microorganisms survive in sheltered geological niches that allow for biological activity.

  • Dormancy and sporulation are common behavioural responses to desiccation that enable xerotolerant microorganisms to react to sporadic cycles of rainfall and drought by remaining in an inert metabolic state.

  • Xerotolerant bacteria use several physiological mechanisms to prevent cell disruption and water loss, including phospholipid modifications to maintain membrane fluidity, the secretion of water-retaining extracellular polymeric substances (EPS), and the accumulation of compatible solutes that preserve the osmotic potential across the membrane.

  • For xerotolerant microorganisms, DNA and protein stability are crucial to ensure that cellular activity is resumed under favourable conditions. Consequently, most molecular adaptations to xeric stress involve the upregulation of proteins that are stable under low water activity and that preserve the integrity of DNA through physical protection and repair.

  • Although xerotolerant bacteria are unique in their capacity to survive in environments in which water is scarce, many of the adaptive mechanisms that they use are also triggered by other abiotic stresses that are present in these environments. Therefore, these mechanisms are part of broader adaptive response that enables the survival of microorganisms in extreme biomes.

Abstract

Water is vital for many biological processes and is essential for all living organisms. However, numerous macroorganisms and microorganisms have adapted to survive in environments in which water is scarce; such organisms are collectively termed xerotolerant. With increasing global desertification due to climate change and human-driven desertification processes, it is becoming ever more important to understand how xerotolerant organisms cope with a lack of water. In this Review, we discuss the environmental, physiological and molecular adaptations that enable xerotolerant bacteria to survive in environments in which water is scarce and highlight insights from modern 'omics' technologies. Understanding xerotolerance will inform and hopefully aid efforts to regulate and even reverse desertification.

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Figure 1: Effects of desiccation on the physiology and biochemistry of bacterial cells.
Figure 2: Niches of xerotolerant communities.
Figure 3: Adaptive mechanisms of xerotolerant bacteria.
Figure 4: Dormancy and evasion of environmental stress.

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Authors and Affiliations

  1. Department of Genetics, Centre for Microbial Ecology and Genomics (CMEG), University of Pretoria, Hatfield, 0028, Pretoria, South Africa

    Pedro H. Lebre & Don A. Cowan

  2. School of Molecular and Cell Biology, University of the Witwatersrand, Private Bag 3, Wits, Johannesburg, 2050, South Africa

    Pieter De Maayer

Authors
  1. Pedro H. Lebre
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  2. Pieter De Maayer
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  3. Don A. Cowan
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Correspondence to Don A. Cowan.

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FURTHER INFORMATION

MG-RAST metagenomics repository

PowerPoint slides

Glossary

Hypertonicity

A solution that contains a higher concentration of solutes than another solution.

Hyper-arid

An oligotrophic environment with severe water shortage, low precipitation and soil erosion that poses extreme challenges to the survival of living organisms. Technically, hyper-arid environments have an aridity index of less than 0.05.

Water activity

(aw). A measurement of the water that is available to an organism in the environment. It is calculated as the ratio of the vapour pressure in an environment relative to pure water under identical conditions.

Maillard reactions

Non-enzymatic reactions in which the reactive carbonyl groups of sugars react with primary amines of nucleic acids and amino groups of proteins, forming covalent bonds that cause crosslinks between proteins and DNA. These reactions are also referred to as Browning reactions.

Hydroxyl radicals

The neutral form of the hydroxide ion (OH−).

Metataxonomic approaches

(MTX approaches). The high-throughput sequencing of taxonomic markers (such as 16S rRNA genes) in metagenomic DNA from an environmental sample and the subsequent phylogenetic and taxonomic analyses of the microbial community composition and structure.

Akinetes

Thick-walled dormant cells that are formed through the enlargement of vegetative cells in non-sporulating cyanobacteria and green algae.

Monoenoic fatty acids

An unsaturated fatty acid that has only one double bond.

Cyclopropane fatty acids

Rare fatty acids that are produced through the cyclopropanation of unsaturated fatty acids.

Hexagonal II phase

A membrane lipid polymorphism in which lipids aggregate into cone shapes that are organized with the polar head groups on the inside of the cone and the hydrophobic hydrocarbons tails on the outside. The creation of these aggregates increases the packing disorder of lipid membranes under xeric stress.

Phosphatidylglycerol lipids

Glycerophospholipids that consist of an L-glycerol-3-phosphate backbone ester-linked to either saturated or unsaturated fatty acids at carbon 1 and carbon 2.

Cardiolipin

A negatively charged diphosphatidylglycerol lipid that consists of a glycerol backbone linked to two phosphatidic acid moieties.

Halophiles

Organisms that are adapted to thrive in environments that have saturated salt content and do not grow optimally in more mesophilic environments.

Vitrification

The formation of glass by disaccharides (such as trehalose and sucrose), which is induced by the removal of water from the intracellular environment. The decrease in diffusion rates inside the cell caused by vitrification is thought to be crucial for resistance to water stress, as it slows down diffusion rates and prevents the accumulation of harmful reactive oxygen species (ROS).

Glyoxylate shunt

A variant of the tricarboxylic acid (TCA) cycle that involves the conversion of acetyl-CoA to succinate for the biosynthesis of carbohydrates.

Chemotaxis

A process that is carried out by a system of membrane chemoreceptors and signal-transducing pathways that controls the ability of bacteria to move by means of flagella towards attractants and away from repellents.

Housekeeping proteins

Proteins that are necessary for normal cellular functions and are typically encoded by constitutively expressed genes.

Catalases

Enzyme that are common to all domains of life that catalyse the degradation of hydrogen peroxide to water and oxygen.

Thioredoxins

A class of small proteins that are involved mainly in redox signalling.

Alternative sigma factors

Specialized sigma factors that react to external environmental triggers and regulate specific cell functions, such as stress tolerance, flagellar motility and virulence.

Type III secretion system

Protein machinery found in the Gram-negative bacteria that secretes effector proteins that assist in the infection of eukaryotic hosts.

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Lebre, P., De Maayer, P. & Cowan, D. Xerotolerant bacteria: surviving through a dry spell. Nat Rev Microbiol 15, 285–296 (2017). https://doi.org/10.1038/nrmicro.2017.16

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