Endolithic microbes of rocks, their community, function and survival strategies

Highlights

• Diverse microbial communities colonize inside rocks to avoid ecological stresses.

• Rocks weathering and minerals dissolution is their key biochemical functions.

• This offers a model system for unique microbial ecology, astrobiology, and geobiology.

• Endolithic remnants act as biosignatures and offer evidence about Martian life.

Abstract

Endolithic micro-environments of rock are unique, ranging from high mountains and deep-sea floors to deserts and the Arctic and Antarctic regions colonized by high diversity of microbes. Endolithic microorganisms survive the extreme environmental conditions of rock pores and fissures with their survival strategies. In addition, the bulk rock provides mineral nutrients and protects the inhabitants from drastic ecological stresses from changes in the local conditions. Thus, endolithic microbes are at pivotal interface between geology and biology that offers a model system for unique microbial ecology, astrobiology, and geomicrobiology. This review provides comprehensive information on the diversity of endolithic microbial communities in cold, arid, aquatic, and terrestrial ecosystems and their survival strategies under ecological stresses. Furthermore, rock architecture for the colonization of endoliths, their biochemical functions and potential applications are discussed. It is clear that integrating modern molecular methods with physical and chemical analytical instrumentation will further advance our knowledge about endolithic microbial ecology, diversity, unique adaptive mechanisms, ecological functioning, and biochemical processes that shape the past, current, and future biosphere.

Introduction

Microbes have 3.4 billion years of history (Meslier and DiRuggiero 2019). Microorganisms inhabit nearly all imaginable parts of the Earth. According to Dutch microbiologist Lourens Baas-Becking, microorganisms can reach every corner of the Earth but only grow in suitable habitats (Baas-Becking 1934), including rocks. Microorganisms that colonize inside rocks are endolithic (Makhalanyane et al., 2014; De Los Ríos et al., 2014a). Rocks are natural aggregates of minerals and mineral-like ingredients called mineraloids. Mainly, rocks are oligotrophic environments still microbial life can sustain here (Table 1). Bioreceptivity is the ability of any material surface to be colonized by microbes depending on several surface properties (Guillitte 1995). The chemical and physical properties of rocks significantly affect their bioreceptivity (Warscheid and Braams 2000). Endolithic microorganisms create a vital interface between geology and biology by inhabiting distinctive ecological niches within rocks of marine, freshwater, and terrestrial environments. Endoliths include several types of rocks, including hard granite (Schultz et al., 2000; De los Robinson et al., 2015; Archer et al., 2017), porous ones including sandstone and limestone (Friedmann 1982; Tschermak-Woess and Friedmann 1984; Gross et al., 1998; Matthes et al., 2001; Wierzchos and Ascaso 2001; Coleine et al., 2021). Endoliths are classified into (i) cryptoendolith; when living in the natural structural cavities, (ii) chasmoendoliths; growing in the cracks and fissures of the rock, (iii) euendoliths; organisms that actively penetrate the rocks and produce new cavities and tunnels and promote biogenic weathering of rocks, and (iv) autoendoliths; organisms that contribute in the deposition of mineral on the rock (Golubic et al., 1981; Marlow et al., 2015) as shown in Fig. 1a. However, this classification is not mutually exclusive since lichens could be both endolithic and epilithic at the same time, and also organisms can colonize in preexisting pores as chasmoendolithic or cryptoendolithic and perform rock weathering like endoliths (Amarelle et al., 2019). Endoliths are the significant components of the food chain (Hutchings 1986; Radtke et al., 1996). Colonization of endoliths is mostly visual as colored bands are present in a parallel pattern to the rock surface, having photosynthetic microbes alternating with fungal-dominated strata (Friedmann 1982; De Los Ríos et al., 2014a). The exposed surface of rock (a few millimeters to centimeters) creates a significant microbial ecosystem by colonizing photosynthetic microbial communities (Fig. 1b). To inhabit a rigid substrate, endolithic microbes can adopt two strategies: constructive embedment and destructive bioerosion (Tapanila and Ekdale 2007). The endolithic ecosystem is one of the simplest microbial ecosystems that provide a manageable model for testing the ecological principles that are mostly untested in the microbial ecology due to limitations in experiments and extraordinary microbial diversity (Pace 1997). Endoliths contribute to vital geological processes such as bioerosion of calcareous and limestone substrates, synthesis of fine-grain sediments (Torunski 1979), modification by micritization (Schneider and Torunski 1983), and transformed silicate rocks and soil formation on Earth (Mergelov et al., 2018).

Planet Earth consists of several known environmental conditions with simultaneous and multiple forms of stresses, which regulate the boundaries of life (Wierzchos et al., 2018). These environments are physiochemically polyextreme and might inhabit by polyextremotolerant and polyextremophilic microorganisms. One such polyextreme environment is the rocks that contain a network of fissures and pores, which linked the rock surface in the translucent rock (Nienow 2009) and colonized by endoliths. This colonization is a survival strategy and the overlying rock mineral protect the endoliths from thermal buffering, lethal ultraviolet (UV) radiations, freeze-thaw events, enhance moisture availability and physical stability (Pointing and Belnap 2012; Wierzchos et al., 2012a; De Los Ríos et al., 2014b; Wierzchos et al., 2018). Therefore, the endolithic mode of life provides a living advantage in a hard domicile protected from biological and physical stresses and broadens the range of habitats for endoliths in a unique ecospace. Furthermore, fossil traces recorded in the rocks exhibited that stable residence is essential for microorganisms (Tapanila 2008). These facts encouraged US National Aeronautics and Space Administration (NASA) to trace life on Mars.

Endoliths include nonphotoautotrophic bacteria, fungi, red and green algae, Cyanobacteria, and lichen. Groups of these organisms colonize most endolithic habitats, and diversity of non-photoautotrophic bacteria is present (McNamara et al., 2006). The oldest endolithic microorganisms identified as Cyanobacteria, preserved in silica and discovered in 1500 million years' ancient rocks from Dahongyu Formation in China (Zhang and Golubic 1987). Yang et al. (2017) discovered euendolithic Cyanobacteria (Endoconchia lata) in skeletal and embryo-like fossils collected from the Lower Cambrian Kuanchuanpu Formation (ca. 535 Ma), Shaanxi, China. These euendoliths were preserved as phosphatic casts on the surface of moulds or steinkerns of small skeletal fossils. Endoliths enabled researchers to study how microorganisms travel the Earth (Smith et al., 2013) and how they could exist on other planets (Dance 2015). The diversity of endolithic microbes, especially bacteria and archaea, their metabolic potentials, interaction patterns with biotic and abiotic components of the ecosystem are largely unknown. Endolithic habitat is one of the polyextremophilic habitats that provide a unique genomic pool and the best model of several biochemical, physiological, and molecular survival strategies and resistance of their inhabitants. In addition, endolithic microorganisms are essential to be explored for the evolution of the mineral within rocks, their role in Earth's geochemical cycles and geological records, and providing insight into the origin of life on this planet. Preserved endolithic remnants could be biosignatures for past life and provide information about extraterrestrial life and can be helpful to address the long-lived query, are we alone? We reviewed the endolithic bacterial communities discovered in different habitats and adapted strategies against extremely harsh environmental conditions. In addition, potential applications of the endolithic bacteria reported from these unique ecospaces in microbial ecology, astrobiology, and geobiology are discussed. To further understand the microbial ecology and ecological function of endoliths, integrating contemporary molecular approaches with high-energy microscopy and spectroscopy is crucial to be employed.