Beyond the extremes: Rocks as ultimate refuge for fungi in drylands

Abstract

In an era of rapid climate change and expansion of desertification, the extremely harsh conditions of drylands are a true challenge for microbial life. Under drought conditions, where most life forms cannot survive, rocks represent the main refuge for life. Indeed, the endolithic habitat provides thermal buffering, physical stability, and protection against incident ultraviolet (UV) radiation and solar radiation and, to some extent, ensures water retention to microorganisms. The study of these highly specialized extreme-tolerant and extremophiles may provide tools for understanding microbial interactions and processes that allow them to keep their metabolic machinery active under conditions of dryness and oligotrophy that are typically incompatible with active life, up to the dry limits for life. Despite lithobiontic communities being studied all over the world, a comprehensive understanding of their ecology, evolution, and adaptation is still nascent. Herein, we survey the fungal component of these microbial ecosystems. We first provide an overview of the main defined groups (i.e., lichen-forming fungi, black fungi, and yeasts) of the most known and studied Antarctic endolithic communities that are almost the only life forms ensuring ecosystem functionality in the ice-free areas of the continent. For each group, we discuss their main traits and their diversity. Then, we focus on the fungal taxonomy and ecology of other worldwide endolithic communities. Finally, we highlight the utmost importance of a global rock survey in order to have a comprehensive view of the diversity, distribution, and functionality of these fungi in drylands, to obtain tools in desert area management, and as early alarm systems to climate change.

Mars: new insights and unresolved questions

“…Specialized microbes able to exploit this habitat on Earth by developing in the airspaces of rocks are protected from intense solar radiation and desiccation, allowing their population to persist even in the most-extreme terrestrial climates (Walker et al, 2005). Endolithic microorganisms are often the predominant form of life in hot-and cold deserts (Coleine et al, 2021), including the McMurdo Dry Valleys of Antarctica characterized by extreme cold-and arid conditions, along with the intense UV irradiation reaching ground level (Onofri et al, 2004;Bernhard and Stierle, 2020). Therefore, they have value as Mars analogue sites (Friedmann, 1982;Selbmann et al, 2018).…”

Environmental thresholds in the functional mycobiome of global drylands

“…Conversely, putative plant pathogens were mostly dominated by ascomycetes from the classes Dothideomycetes and Leotiomycetes, which are known to possess unique physiological traits allowing them to resist environmental stresses typical of drylands, including UV radiation, high temperature fluctuations and dissection 7,9,25 . Such common traits might allow potential pathogens from these taxonomic groups to adapt to a wide range of environmental stressors, possibly explaining the ability of the members of this ecological group to thrive in extreme environments.…”

“…Fungi are paramount components and drive critical ecosystem services in drylands, contributing to the formation of fertile islands 4 , nutrient cycling and climate regulation 5 , with a major role in dryland primary production 6 and pedogenesis 7 . Key fungal groups include pathogens, mutualistic symbionts of both plants and animals, lichenized fungi, as well as soil and litter saprobes.…”

Endolithic microbial composition in Helliwell Hills, a newly investigated Mars‐like area in Antarctica

“…Cryptoendolithic microbial communities are self‐sustaining ecosystems and almost the only specialized life‐forms spreading in these areas, maintaining functionality under conditions at the limits for supporting life, as main contributors to biogeochemical processes. The hard nature of rock substratum guarantees physical stability and also provides thermal buffering, protection against UV radiation and excessive solar radiation and water retention, enabling microorganisms to endure environmental conditions that are normally incompatible with an active life (Coleine et al ., 2020a). Cryptoendoliths normally live in strict spatial association forming microbial communities; the most studied and widespread in Antarctica is the lichen‐dominated community, typically occupying a niche in a few millimetres depth below rock surface (Friedmann, 1982).…”