Abstract
Lithic-associated microhabitats, referred to as lithobiontic ecological niches and their communities are termed lithobionts. Lithic niches are widely dispersed in Antarctica and allow microbial communities to circumvent environmental stressors such as temperature fluctuations, low moisture levels, and high ultraviolet radiation. Here, we assess the status of research on the three recognized classes of lithobiont communities (epiliths, hypoliths and endoliths). We describe the microbial diversity of lithobionts, the factors that influence colonization, and the roles played by these communities in the Antarctic soil ecosystem. In order to understand community dynamics, such as beta-diversity patterns and factors that drive them, we advocate the application of “omics-based approaches” that can reveal both the functional capacities and adaptive potentials of complex microbial communities.
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Keywords
- Extracellular Polymeric Substance
- Terminal Restriction Fragment Length Polymorphism
- Cold Desert
- Rock Substrate
- Polar Desert
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
9.1 Introduction
The ice-free polar desert landscapes of Antarctica present an extremely challenging environment for life. Severe thermal, moisture and UV stress is exacerbated by an ultraoligotrophic terrestrial landscape that is comprised largely of mineral soils and rocks (Cary et al. 2010). Higher plants and animals are absent from this environment, and instead, the biotic component of this ecosystem is almost exclusively microbial (Cowan and Tow 2004). The largest and best understood of the ice-free regions is the McMurdo Dry Valleys (Fig. 9.1), and this hyperarid desert supports vast expanses of exposed rocky substrate. Microbial colonization of various rock substrates occurs, although this is cryptic and not readily observed on many surfaces. These lithic-associated microhabitats are referred to as lithobiontic ecological niches, and their communities are termed lithobionts (Golubic et al. 1981). Numerous studies have shown that lithobionts [also referred to as soil rock surface communities (SRSCs)] are widespread in both hot and cold deserts and are often the only visible life in such extreme terrestrial environments (Pointing and Belnap 2012). These communities are thought to contribute significantly to the ecology and function of both hot and cold deserts.
In this chapter, we review the status of research on the three recognized classes of lithobiont communities (Fig. 9.2): epiliths adhere to the surface of the rock, endoliths are found within the rock matrix, and hypoliths attach to ventral rock surfaces. We describe the microbial diversity of lithobionts, factors that influence colonization and the role played by these communities in the Antarctic ecosystem.
9.2 Lithobiontic Ecological Niche
The three lithobiontic niches are delineated largely as a function of the mineral substrate. Epiliths are perhaps the least fastidious and occur on various igneous rock surfaces. Endolithic colonization is restricted to porous sandstones and weathered granitic rocks, while hypoliths generally develop beneath translucent quartz and marble rocks (Pointing and Belnap 2012). Examples of epilithic, endolithic and hypolithic colonization are shown in Fig. 9.1.
9.2.1 Epiliths
Epilithic organisms populate the surfaces of stable rock substrata with access to sufficient quantities of moisture (Wynn-Williams 2002; Smith 1982). The establishment of epiliths is often associated with moss and lichen communities on the rock surfaces (Pointing and Belnap 2012; Nash et al. 1977), although heterotrophic fungi and cyanobacteria also appear to be key constituents (Staley et al. 1982; Gorbushina 2007).
Epilithic colonization is perhaps the most vulnerable of the three lithic types, as they are exposed to strong winds, ultraviolet radiation (UVR), desiccation and other perturbations (Cockell et al. 2008; Wynn-Williams and Edwards 2000). As a consequence, epiliths are often restricted to the milder lower latitude Antarctic regions such as Princess Elizabeth Land and Mac Robertson Land (Broady 1981a, 1996; Wynn-Williams and Edwards 2000).
9.2.2 Endoliths
Endolithic microbial communities colonize the interior of rocks by adapting to the different ecological sub-niches within the lithic substrate (Golubic et al. 1981). Depending on the micromorphological and structural properties of the rock, endoliths can be found as interstitial habitats of cracks and fissures (chasmoendoliths or chasmoliths) and also in pore spaces between mineral grains (cryptoendolithic) (Golubic et al. 1981; Nienow and Friedmann 1993; Budel et al. 2009). Chasmoliths are commonly found in siliceous rocks, but also have been reported in granite, marble, silicified sandstone, gypsum crusts and anorthosite (Friedmann 1982; Broady 1981b; de los Rios et al. 2005b). In contrast, cryptoendoliths are principally associated with porous sandstone rocks (Bell 1993; Friedmann and Ocampo-Friedmann 1984; Nienow et al. 2003; Omelon 2008; Sun et al. 2010), but may also be recovered in other suitable mineral types including granite, gneiss, limestone, marble, gypsum, halite and evaporites (Cockell et al. 2002; Nienow and Friedmann 1993; Boison et al. 2004; Wierzchos et al. 2006).
It has been demonstrated that cryptoendolithic microbial communities in Beacon sandstones, in the Antarctic Dry Valleys, promote biogenic weathering of rock substrates, and colonized sandstones show distinct exfoliation patterns on the rock surface (Friedmann and Weed 1987; Nienow and Friedmann 1993). Colonized sandstones display different coloured patches (white, yellow, orange or brown), the result of both the constructive aeolian weathering process and the destructive biogenic weathering process (Sun and Friedmann 1999; Sun et al. 2010). Long-term microbial colonization and the biogenic accumulation of oxalic acid dissolve the cementing substances between the mineral grains, resulting in exfoliation of the surface crust and loss of biomass (Sun and Friedmann 1999). This exfoliative weathering process is cyclic, and each phase is estimated to last for 1 × 104 years (Friedmann et al. 1993; Sun et al. 2010). The process contributes to both the formation of mineral soils and the organic carbon fraction in the soil phase (Nienow and Friedmann 1993).
Chasmoliths are found in both the vertical fissures and horizontal cracks in rocks; the former are common in quartz glacial debris, whereas the latter are common in charnockite (a rare type of granite containing pyroxene) substrates (Vincent 2004). They are also frequently described in the fine fracture zones of marble which is common to the Antarctica landscape (Vincent 2004; Cowan and Ah Tow 2004). Chasmoliths are not exclusive to Antarctica, and they have been reported from other deserts in central Asia, central Australia, south-western USA and Mexico (Broady 1981b; Friedmann et al. 1967; Friedmann and Ocampo-Friedmann 1984).
9.2.3 Hypoliths
Hypolithic microbial communities (hypolithons) inhabit the ventral surfaces of rock substrates at the rock–soil interface (Friedmann et al. 1967; Golubic et al. 1981). Hypolithons typically colonize translucent rocks such as quartz, gypsum and granite (Broady 1981a, b) but may also be found under opaque rocks (e.g. dolomite and gneisses) (Cockell and Stokes 2004, 2006). As with endoliths, hypolithic communities are dominated by photoautotrophs such as cyanobacteria, which require a minimum level of photosynthetically active radiation (PAR) for photosynthesis (discussed below) (Friedmann et al. 1993).
In an observational study, three types of hypolithic communities were reported in the Miers Valley: the cyanobacterial dominated (Type I), the fungal dominated (Type II) and the bryophyte dominated (Type III) (Cowan et al. 2011a, b). The morphological characteristics of growth in these communities differ, and the hypolithons may be either loosely attached to the rock or unattached depending on the main community components. Type I hypoliths adhere directly to the rock forming a biofilm composed primarily of filamentous oscillatorian cyanobacterial morphotypes (Pointing et al. 2009). Type II communities comprise a filamentous network structure cemented to the rock surface, while the macroscopic moss structures of Type III communities are embedded in the soil under the translucent rock (Cowan et al. 2010a). These hypolithic types are both morphologically complex and diverse in composition. The community structures of hypolithic communities has recently been determined using amplified RNA intervening sequence analysis (ARISA), terminal restriction fragment length polymorphism (T-RFLP), clone library construction and pyrosequencing analysis of the 16S rRNA gene phylogenetic market gene (Wood et al. 2008; Pointing et al. 2009; Cowan et al. 2011a, b; Makhalanyane et al. 2013a).
9.3 Establishment of Lithobiontic Communities
Lithic communities have been described associated with a variety of substrates, including fine-grained Beacon sandstone, limestone, gypsum and flint (Nienow and Friedmann 1993; Cowan et al. 2010c; Cary et al. 2010; Cockell and Stokes 2004). Colonization of the rock is thought to depend on a combination of abiotic factors including macro- and microclimate (discussed below), ultrastructure, mineral composition and pH, which together contribute to the ability of the rock to host microorganisms (Friedmann and Ocampo-Friedmann 1984). Biotic factors are also involved during the colonization process. For instance, cyanobacteria are known to dominate habitats with high pH values and high levels of calcium and magnesium carbonates (Johnston and Vestal 1989). Fungal-dominated habitats have been reported from high altitude locations with high metal oxide concentrations (Connell et al. 2006; Pointing et al. 2009).
9.3.1 Temperature
The temperature of the lithobionts has been found to be closely linked to the ambient air temperature and the level of solar radiation (Nienow and Friedmann 1993). However, thermal buffering, due to the black body absorption effect of opaque rocks or the “greenhouse effect” of translucent quartz rocks, has been detected (Friedmann 1980; McKay et al. 2003; Schlesinger et al. 2003; Wynn-Williams 2002; Cowan et al. 2011a, 2010c). Daytime peak rock-air temperature differences in the Antarctic Ross Desert and in the Sonoran Desert in North America were 15 and 10 °C, respectively, indicating similar trends for both hot and cold deserts (Friedmann 1980; McKay and Friedmann 1985). However, three recent studies (Azua-Bustos et al. 2011; Makhalanyane et al. 2013b; Tracy et al. 2010) measuring microclimatic variables in hypolithons from hot deserts reported lower temperatures at the rock surface interface in daytime and night-time, and warmer night-time temperatures when compared to open soil in conflict with earlier studies (Schlesinger et al. 2003).
Depending on a number of factors including aspect, elevation and other geographical features, the annual temperatures in the McMurdo Dry Valleys ranges from −14.8 to 30 °C, with differences between the maximum and minimum of approximately 50 °C (Doran et al. 2002). These extreme temperature ranges impose severe freeze–thaw stresses on microorganisms (Nienow et al. 1988). Therefore, it has been hypothesized that the thermal buffering provided by rocks is perhaps most significant in polar deserts as lithobionts are protected from rapid freeze–thaw stress (Wynn-Williams 2002; Cowan et al. 2010c, 2011a). The effect of katabatic wind episodes, which have a direct effect on both temperature fluctuations and the physical stability of soil crusts, is also minimized by the lithobiontic lifestyle. Reports suggest that surface rock temperature can be up to 20 °C higher than ambient air temperatures during sunny periods (Kappen et al. 1983). The warmer rock mass may also prolong the period of lithophytic microbial growth in polar deserts during polar summers (Wynn-Williams 2002).
9.3.2 Water Availability
The rock microhabitat has been shown to offer improved water availability compared to the surrounding soil (Tracy et al. 2010; Cowan et al. 2010c; Chan et al. 2012; Warren-Rhodes et al. 2006). In rainfall zones (such as the Antarctic Peninsula), the overlying rock provides protection from raindrop impact during precipitation, but provides a narrow annuli of unsealed soil near the sheltered margins of stones, that serve as sites for water entry and air escape for lithic niches (Thomas 1997). The rock also serves as a collector of water during precipitation, fog and dew events (Warren-Rhodes et al. 2006).
Liquid water is an essential requirement for the development of epilithic colonists. Increases in precipitation have been reported to lead to surges in cover and biomass (Broady 1996, 1989). As a result, epilithic colonization is highest at moist coastal areas and locations with frequent irrigation by snowmelt or high atmospheric humidity, and around bases of nunataks where exposed rocks meet surrounding ice fields (Broady 1981b, 1989, 1996). The diversity of Antarctic epiliths has been reported to drop significantly along moisture gradients. For example, the total lichen species diversity was found to decrease from 18 genera in Dronning Maud Land (approximately 200 km inland) to only 5 genera a further 1,000 km from the coast in the Pensacola Mountains (Cameron 1972; Engelskjøn 1986; Wynn-Williams 2002).
Hypolithons access water from rainwater runoff collected and from condensation on the rock surface during fog and dew events (Bullard 1997; Warren-Rhodes et al. 2006). The overlying rock also serves as a physical impediment to evaporation (Wynn-Williams 2002). The water content of Dry Valleys soils below hypolithon-colonized rocks has been shown to range from 6 to 14 % w/w, with open soils containing significantly less moisture (0.5–2 % w/w) (Smith et al. 2000). Other factors, such as porosity of the rock, have also been shown to help retain moisture (see below) (Friedmann 1980; Kappen et al. 1983).
Water availability in soil has been shown to regulate the upper boundary for growth, while the lower boundary is determined by the light regime, controlled by the translucence of the overlying rock substrate. In Antarctic hypoliths, quartz rocks have been reported to effectively filter UVA and UVB radiation, both potentially detrimental to colonization (Cowan et al. 2010c). Moisture also improves light transmittance through the rock, because light scattering is reduced when all air spaces between mineral particles are filled with water (Vincent 2004).
Extracellular polymeric substances (EPS) have been described for several lithobiontic communities (de los Ríos et al. 2003, 2005a; Pointing and Belnap 2012). The role of EPS is thought to be essential in terms of water relations in lithobionts. Both composition and hygroscopic properties provide a matrix for water absorption and retention and for absorbing organic compounds and ions. de los Rios et al. (2004) have speculated that EPS may be essential both for preserving the microbial populations in lithobionts and for facilitating photosynthesis in endolithic cyanobacteria. Microbial EPS can also promote soil fertility, as the components of the matrix create a mosaic of polyfunctional binding sites that retain excess heavy metals while concentrating growth-promoting nutrients on the sheath (Gadd 1990). The collection and absorption of dew by hypolithons have been quantitatively correlated with EPS abundance (Gorbushina 2007).
9.3.3 Light Availability
The translucence of the rock substrate is critical for refuge lithobiont colonization and growth. Although light transmission through the quartz pebbles of 13–80-mm thickness was filtered to 0.9–2.7 % of the incident sunlight (Broady 1981b), the presence of cyanobacterial-dominated microbial communities is tangible evidence that such low light levels are sufficient to support photoautotrophic processes. Porosity and translucence of the rock substrate are the most important properties which enable colonization in endoliths (Cowan and Ah Tow 2004). The interior surfaces of the rock are characterized by a steep light gradient along depth due to light attenuation by rock substrates (Friedmann 1980). The porosity of rocks ranges from 0 to 50 % and is influenced by many factors such as rock type, the mineral content and grain particle size (Šperl and Trčková 2008).
In the polar regions, it has been reported that the hypolithic colonization of opaque rocks was promoted by local periglacial activities (the freezing and thawing of ground water) which sort rocks and stones into polygonal spatial arrangements, creating openings around the margins of quartz rocks and facilitating the penetration of light to the undersides (Cockell et al. 2002; Cockell and Stokes 2004). The attenuation of light by rocks also assists microbial colonization by effectively reducing UVR stress in refuge lithic niches (Broady 1981b; Cowan et al. 2010c; Wong et al. 2010a).
The extent of light penetration through different rock substrates has been found to determine the abundance of hypolithic colonizations under translucent and opaque rocks (Berner and Evenari 1978). For instance, colonizations under translucent rocks were mostly observed <25 mm thick and up to 40 mm thick, while lower abundances were observed under opaque rocks, generally of <15 mm and up to 30 mm thick (Berner and Evenari 1978). Other authors, e.g. Nienow and Friedmann (1993), found that hypolithic colonizations below quartz rocks ranged from several mm to 60 mm in depth. Microbial colonization beneath thicker rocks is confined to the periphery, as insufficient light to support photosynthesis is transmitted to the community at the base of the rock (Broady 1981b; Schlesinger et al. 2003).
9.4 Microbiology of Lithobionts
Lithobiontic diversity analysis was initially based on microscopic observations of morphological and ultrastructural features of cultured isolates (Friedmann 1980; Friedmann et al. 1988). More recently, culture-independent approaches have allowed a more comprehensive and representative knowledge of the composition of lithobiontic microbial communities (Khan et al. 2011; Smith et al. 2006; Pointing et al. 2009; Chan et al. 2013; Babalola et al. 2009; Makhalanyane et al. 2013a).
9.4.1 Epilith Diversity
Very little is currently known about epilithic microbiology, compared to the endolithic and hypolithic niches. By using culture-dependent approaches we know that Chroococcidiopsis, Myxosarcina, Gloeothece, Plectonema, Lyngbya and Calothrix species are commonly found in epilithic communities in Princess Elizabeth Land and Mawson Rock (Broady 1981a, b). In the same geographical area, 13 epilithic cyanobacterial species were identified (Broady 1989). Epiliths appear to be dominated by cyanobacterial taxa, perhaps as a consequence of their abilities to withstand UV irradiation (Campbell et al. 1998; Castenholz and Garcia-Pichel 2002). Further work, employing modern metagenomic approaches, is required to understand the “true” diversity of epilithic communities.
9.4.2 Endolith Diversity
Free cyanobacteria, together with lichenized structure, have been found to dominate endolithic communities (Friedmann et al. 1988). The cyanobacterium Choroglea sp. was detected in translucent gypsum crusts formed on sandstone surfaces on Alexander Island (Hughes and Lawley 2003). In the Taylor Valley, different genera of cyanobacteria, mainly Chrocooccidiopsis sp. with some Cyanothece cf. aeruginosa and Nostoc sp. (Büdel et al. 2008), have been identified. Cyanobacteria of the genera Gloeocapsa were first described in Victoria Land (Friedmann et al. 1988). Later, Friedmann et al. (1988) distinguished and characterized the diversity of the two types of cryptoendolithic communities inhabiting the Ross Desert: lichen-dominated and cyanobacterial communities. A total of 17 cyanobacteria from the McMurdo Dry Valleys were described. Depending on the dominant cyanobacterium, three communities were observed: Gloeocapsa, Hormathonema–Gloeocapsa and Chroococcidiopsis.
Using molecular techniques, lichenized endolithic communities were shown to be dominated by a single green algal species Trebouxia jamesii (de la Torre et al. 2003). T. jamesii is a known constituent of lichen associations, such as the lichenized fungal genus Letharia (Friedl and Rokitta 1997).
The analysis of the prokaryotic members of the community showed a diverse range of phylotypes related to Actinobacteria, α- and γ-Proteobacteria and Planctomycete species, and an abundance of uncultured bacteria (de la Torre et al. 2003). Clone libraries from endolithic communities showed a high actinobacterial diversity. Endoliths were dominated by cyanobacteria of the Chroococcidiopsis lineage (Friedmann 1982) and cyanobacteria morphologically similar to Gloeocapsa, Plectonema and Hormathonema species (Pointing et al. 2009; Wong et al. 2010b; de la Torre et al. 2003; de los Rios et al. 2004, 2005b).
9.4.3 Hypolith Diversity
The community structure and prokaryote species diversity of hypoliths are the best understood of all the lithobionts (Bahl et al. 2011; Chan et al. 2012, 2013; Cowan et al. 2010b; Khan et al. 2011; Makhalanyane et al. 2013b; Pointing et al. 2009). The prokaryotic composition of Antarctic hypolithons has been assessed using a range of approaches.
A combination of microscopy and culture-independent approaches has identified cyanobacteria as the predominant phylum in hypolithic colonization globally (Bahl et al. 2011; Lacap et al. 2010; Pointing et al. 2007; Stomeo et al. 2013; Warren-Rhodes et al. 2007), including Antarctica’s McMurdo Dry Valleys and other ice-free areas (Broady 1981b, 2005; Smith et al. 2000; Pointing et al. 2009). Morphological studies suggest that cyanobacteria found in Antarctica and other cold deserts are dominated by filamentous oscillatorian morphotypes, with a lower species richness than other deserts (Smith et al. 2000; Chan et al. 2012). Communities in the Vestfold Hills showed the presence of oscillatorian cyanobacteria with morphologies typical of the Lyngbya/Phormidium/Plectonema group and coccoid cells morphologically similar to Chroococcidiopsis (Smith et al. 2000). Hypolithic communities have also been shown to harbour other bacterial phyla such as Actinobacteria, α- and β-Proteobacteria, Planctomycetes, Firmicutes, Acidobacteria and Verrumicrobia (Makhalanyane et al. 2013a; Bahl et al. 2011; Caruso et al. 2011). Archaeal phylotypes recovered were phylogenetically affiliated with a large group of uncultured Crenarcheota (Khan et al. 2011).
Although the majority of studies have focused on the bacterial composition in these communities (Bahl et al. 2011; Caruso et al. 2011; Makhalanyane et al. 2013a; Wood et al. 2008), there is evidence that the eukaryotic composition is more complex than initially anticipated (Khan et al. 2011; Gokul et al. 2013; Pointing et al. 2009). Eukaryotic phylotypic analysis showed that free-living ascomycetous fungi, chlorophytes and mosses were present in hypolithons (Khan et al. 2011). A detailed study focusing on the microeukaryotes in all three Antarctic hypolith types reported populations of novel uncharacterized Bryophyta, fungi and protists (Gokul et al. 2013). The presence of these taxa suggests that hypoliths may harbour quite complex food webs and therefore may be important in the cycling of nutrients in the cold desert oligotrophic environment.
Interestingly, it has been suggested that the different Antarctic hypolithic community morphotypes represent sequential stages of succession (Makhalanyane et al. 2013b; Cowan et al. 2010b). The bacterial community compositions of the three hypolith types in the east Antarctic Miers Valley show separate and statistically significant clustering. Using a probabilistic dissimilarity matrix analysis (Makhalanyane et al. 2013b), the species composition (beta-diversity) was shown to vary between different sites and was found to be higher in Type I hypolithons than in Types II and III. These differences suggest that deterministic processes in the bacterial component of hypolithons might increase in the order Type I => Type II => Type III. As it is currently assumed that the effects of stochastic variation may become less important as communities develop over time (Fierer et al. 2010), these findings suggest that the Type I (cyanobacteria-dominated) hypolithic community might be the founder community in the succession process. These patterns have important implications as communities of higher beta-diversity are likely to be vulnerable to climate change (McKnight et al. 2007).
9.5 The Role of Lithobionts in Depauperate Environs
Lithobionts are widely dispersed in depauperate environments (Broady 1981b, 2005; Pointing and Belnap 2012; Chan et al. 2012), and in Antarctic terrestrial ice-free environments lithobiontic are often the only primary producers. Hypoliths, which are by far the most widely distributed Antarctic lithobionts, were shown to cover up to 66 cm2 m−2 in some regions and contributed up to 0.85 mg chlorophyll m−2 of total biomass (Broady 1981b). Moreover, in the Arctic, the productivity of hypolithons was estimated to be approximately 0.8 ± 0.3 g m−2. Given the fact that the total average productivity from plants, lichens and bryophytes in the same area was only 1.0 ± 0.4 g m−2 (Bliss et al. 1984), hypolithic productivity was estimated to almost double the productivity estimates (Cockell and Stokes 2004). All together these results suggest hypolithic communities potentially represent a major fraction of the total photosynthetic capacity in Antarctic terrestrial ecosystems.
Hypoliths have also been shown to possess the both the genetic and functional capacity for nitrogen fixation (Cowan et al. 2011b). Nitrogenase activity, determined using the acetylene reduction assay, estimated that total contribution of hypolithic communities to the Miers Valley region at approximately 14,200 mmol N year−1 (0.38 kg N year−1), indicating that these communities are important contributors to fixed nitrogen budgets in Antarctic Desert soils. In consequence, the direct contribution of lithic communities to the total carbon and nitrogen turnover in cold desert ecosystems may be highly significant (Cowan et al. 2011b; Hopkins et al. 2009; Chan et al. 2012).
A recent investigation to establish metabolic capabilities in lithobionts (chasmoendoliths, cryptoendoliths and hypoliths) and open soil from the McKelvey Valley, using a metagenomic approach with GeoChip-based functional gene arrays, was able to reveal certain functional traits that drive community assembly and microbial survival (Chan et al. 2013). This study identified, for the first time, the primary metabolic pathways in lithobionts and showed a high level of genetic plasticity in autotrophs, heterotrophs and diazotrophs. Important differences were found between the open soil, hypolithic and endolithic communities, with new pathways reported for stress-, thermal-, osmotic-responses and nutrient limitation in lithobionts (Chan et al. 2013). The results of this study add substantially to our knowledge of the critical roles played by lithobionts in the Antarctic Desert ecosystem.
9.6 Concluding Remarks
The apparent simplicity of lithobiontic communities makes them good model systems for studies assessing community origins and evolution, trophic functioning and interspecies relationships, and for addressing wider ecological questions. For example, understanding the assembly patterns in hypoliths could shed light on how microbial guilds in other environments might respond to different stressors. Lithobionts may also be good markers for aridity and climate change and may also serve as “ecosystem engineers” (Chan et al. 2012).
Since the initial explorations of the Antarctic lithobiontic ecological niche, we understand considerably more about the microbial diversity within these communities. We are, however, only beginning to learn about their community function and community dynamics, i.e. beta-diversity patterns and the factors that drive them. Modern “omics-based” approaches are potentially very valuable in revealing both the functional capacities and adaptive potentials of microbial communities. For instance, the coordinated use of proteomic and transcriptomic methods could give insight into key metabolic functions and their responses to macro- and microenvironmental changes. There are, however, severe methodological limitations, not the least that both biomass levels and intrinsic process rates are typically low in in situ Antarctic Desert communities. Such limitations notwithstanding, an understanding of the functional guilds in Antarctic lithobiont communities has a particular significance, as these communities are likely to be the basis for the survival of the entire ecosystem.
9.7 Acknowledgements
The authors wish to thank the University of Pretoria, Antarctica New Zealand, the University of Waikato and the South African National Research Foundation SANAP program for supporting field and laboratory research programmes.
References
Azua-Bustos A, Gonzalez-Silva C, Mancilla RA, Salas L, Gomez-Silva B, McKay CP, Vicuna R (2011) Hypolithic cyanobacteria supported mainly by fog in the coastal range of the Atacama Desert. Microbiol Ecol 61:568–581
Babalola OO, Kirby BM, Le Roes-Hill M, Cook AE, Cary SC, Burton SG (2009) Phylogenetic analysis of actinobacterial populations associated with Antarctic Dry Valley mineral soils. Environ Microbiol 11:566–576
Bahl J, Lau MC, Smith GJ, Vijaykrishna D, Cary SC, Lacap DC, Lee CK, Papke RT, Warren-Rhodes KA, Wong FK, McKay CP, Pointing SB (2011) Ancient origins determine global biogeography of hot and cold desert cyanobacteria. Nat Commun 2:6
Bell RA (1993) Cryptoendolithic algae of hot semiarid lands and deserts. J Phycol 29:133–139
Berner T, Evenari M (1978) The influence of temperature and light penetration on the abundance of the hypolithic algae in the Negev Desert of Israel. Oecologia 33:255–260
Bliss L, Svoboda J, Bliss D (1984) Polar Deserts, their plant cover and plant production in the Canadian High Arctic. Ecography 7:305–324
Boison G, Mergel A, Jolkver H, Bothe H (2004) Bacterial life and dinitrogen fixation at a gypsum rock. Appl Environ Microbiol 70:7070–7077
Broady PA (1981a) Ecological and taxonomic observations on subaerial epilithic algae from Princess Elizabeth Land and Mac. Robertson Land. Antarctica. British Phycol J 16:257–266
Broady PA (1981b) The ecology of sublithic terrestrial algae at the Vestfold Hills, Antarctica. British Phycol J 16:231–240
Broady PA (1989) Survey of algae and other terrestrial biota at Edward VII Peninsula, Marie Byrd Land. Antarct Sci 1:215–224
Broady PA (1996) Diversity, distribution and dispersal of Antarctic terrestrial algae. Biodiversity Conserv 5:1307–1335
Broady PA (2005) The distribution of terrestrial and hydro-terrestrial algal associations at three contrasting locations in southern Victoria Land, Antarctica. Algol S 118:95–112
Budel B, Schulz B, Reichenberger H, Bicker F, Green T (2009) Cryptoendolithic cyanobacteria from calcite marble rock ridges, Taylor Valley, Antarctica. Algol S 129:61–69
Büdel B, Bendix J, Bicker FR, Allan Green T (2008) Dewfall as a water source frequently activates the endolithic cyanobacterial communities in the granites of Taylor Valley, Antarctica. J Phycol 44:1415–1424
Bullard JE (1997) Vegetation and dryland geomorphology. Arid Zone Geomorphol, pp 109–131
Cameron RE (1972) Farthest south algae and associated bacteria. Phycologia 11:133–139
Campbell D, Eriksson M-J, Öquist G, Gustafsson P, Clarke AK (1998) The cyanobacterium Synechococcus resists UV-B by exchanging photosystem II reaction-center D1 proteins. Proc Natl Acad Sci 95:364–369
Caruso T, Chan Y, Lacap DC, Lau MC, McKay CP, Pointing SB (2011) Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME J 5:1406–1413
Cary SC, McDonald IR, Barrett JE, Cowan DA (2010) On the rocks: the microbiology of Antarctic Dry Valley soils. Nat Rev Microbiol 8:129–138
Castenholz RW, Garcia-Pichel F (2002) Cyanobacterial responses to UV-radiation. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Kluwer Academic Publishers, The Netherlands, pp 591–611
Chan Y, Lacap DC, Lau MC, Ha KY, Warren-Rhodes KA, Cockell CS, Cowan DA, McKay CP, Pointing SB (2012) Hypolithic microbial communities: between a rock and a hard place. Environ Microbiol 14:2272–2282
Chan Y, Van Nostrand JD, Zhou J, Pointing SB, Farrell RL (2013) Functional ecology of an Antarctic Dry Valley. doi:10.1073/pnas.1300643110
Cockell CS, Stokes MD (2004) Widespread colonization by polar hypoliths. Nature 431:414–414
Cockell CS, Stokes MD (2006) Hypolithic colonization of opaque rocks in the Arctic and Antarctic polar desert. Arct Antarct Alpine Res 38:335–342
Cockell CS, McKay CP, Omelon C (2002) Polar endoliths an anti-correlation of climatic extremes and microbial biodiversity. Int J Astrobiol 1:305–310
Cockell CS, McKay CP, Warren-Rhodes K, Horneck G (2008) Ultraviolet radiation-induced limitation to epilithic microbial growth in arid deserts—dosimetric experiments in the hyperarid core of the Atacama Desert. J Photochem Photobiol B. Biology 90:79–87
Connell L, Redman R, Craig S, Rodriguez R (2006) Distribution and abundance of fungi in the soils of Taylor Valley, Antarctica. Soil Biol Biochem 38:3083–3094
Cowan DA, Ah Tow L (2004) Endangered Antarctic environments. Annu Rev Microbiol 58:649–690
Cowan DA, Tow LA (2004) Endangered antarctic environments. Annu Rev Microbiol 58:649–690
Cowan DA, Khan N, Heath C, Mutondo M (2010a) Microbiology of Antarctic terrestrial soils and rocks. In: Bej AK, Aislabie J, Atlas RM (eds) Polar microbiology: the ecology, biodiversity and bioremediation potential microorganisms in extremely cold environments. CRC Press, Boca Raton, pp 1–29
Cowan DA, Khan N, Pointing SB, Cary SC (2010b) Diverse hypolithic refuge communities in the McMurdo Dry Valleys. Antarct Sci 22:714–720
Cowan DA, Pointing SB, Stevens MI, Craig Cary S, Stomeo F, Tuffin IM (2010c) Distribution and abiotic influences on hypolithic microbial communities in an Antarctic Dry Valley. Polar Biol 34:307–311
Cowan DA, Khan N, Makhalanyane TP, Valverde A (2011a) Antarctic hypolithic communities: model systems for a cryptic astrobiological lifestyle, pp 308–312
Cowan DA, Sohm JA, Makhalanyane TP, Capone DG, Green TGA, Cary SC, Tuffin IM (2011b) Hypolithic communities: important nitrogen sources in Antarctic Desert soils. Environ Microbiol Rep 3:581–586
de la Torre JR, Goebel BM, Friedmann EI, Pace NR (2003) Microbial diversity of cryptoendolithic communities from the McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 69:3858–3867
de los Rios A, Ascaso C, Wierzchos J, Fernandez-Valiente E, Quesada A (2004) Microstructural characterization of cyanobacterial mats from the McMurdo Ice, Shelf Antarctica. Appl Environ Microbiol 70:569–580
de los Rios A, Sancho LG, Grube M, Wierzchos J, Ascaso C (2005a) Endolithic growth of two Lecidea lichens in granite from continental Antarctica detected by molecular and microscopy techniques. N Phytol 165:181–190
de los Rios A, Wierzchos J, Sancho LG, Green A, Ascaso C (2005b) Ecology of endolithic lichens colonizing granite in continental Antarctica. Lichenol 37:383–395
de los Ríos A, Wierzchos J, Sancho LG, Ascaso C (2003) Acid microenvironments in microbial biofilms of Antarctic endolithic microecosystems. Environ Microbiol 5:231–237
Doran PT, McKay CP, Clow GD, Dana GL, Fountain AG, Nylen T, Lyons WB (2002) Valley floor climate observations from the McMurdo dry valleys, Antarctica, 1986–2000. J Geophys Res 107(D24):4772
Engelskjøn T (1986) Botany of two Antarctic Mountain ranges: Gjelsvikfjella and Muhlig-Hofmannfjella, Dronning Maud Land. Polar Res 4:205–224
Fierer N, Nemergut D, Knight R, Craine JM (2010) Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161:635–642
Friedl T, Rokitta C (1997) Species relationships in the lichen alga Trebouxia (Chlorophyta, Trebouxiophyceae): molecular phylogenetic analyses of nuclear-encoded large subunit rRNA gene sequences. Symbiosis Philadelphia Pa 23:125–148
Friedmann EI (1980) Endolithic microbial life in hot and cold deserts. Limit Life 4:33–45
Friedmann EI (1982) Endolithic microorganisms in the Antarctic cold desert. Science 215:1045–1053
Friedmann E, Ocampo-Friedmann R (1984) Endolithic microorganisms in extreme dry environments: analysis of a lithobiontic microbial habitat. In: Klug MJ, Reddy CA (eds) Microbial Ecology. The American Society for Microbiology, Washington, DC, pp 177–185
Friedmann EI, Weed R (1987) Microbial trace-fossil formation, biogenous, and abiotic weathering in the Antarctic cold desert. Science 236:703–705
Friedmann I, Lipkin Y, Ocampo-Paus R (1967) Desert algae of the Negev (Israel). Phycologia 6:185–200
Friedmann EI, Hua M, Ocampo-Friedmann R (1988) Cryptoendolithic lichen and cyanobacterial communities of the Ross Desert, Antarctica. Polarforschung 58:251–259
Friedmann E, Kappen L, Meyer M, Nienow J (1993) Long-term productivity in the cryptoendolithic microbial community of the Ross Desert, Antarctica. Microbiol Ecol 25:51–69
Gadd GM (1990) Heavy metal accumulation by bacteria and other microorganisms. Cell Mol Life Sci 46:834–840
Gokul JK, Valverde A, Tuffin M, Cary SC, Cowan DA (2013) Micro-eukaryotic diversity in hypolithons from Miers Valley, Antarctica. Biology 2:331–340
Golubic S, Friedmann I, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sediment Res 51:475–478
Gorbushina AA (2007) Life on the rocks. Environ Microbiol 9:1613–1631
Hopkins DW, Sparrow AD, Gregorich EG, Elberling B, Novis P, Fraser F, Scrimgeour C, Dennis PG, Meier-Augenstein W, Greenfield LG (2009) Isotopic evidence for the provenance and turnover of organic carbon by soil microorganisms in the Antarctic Dry Valleys. Environ Microbiol 11:597–608
Hughes KA, Lawley B (2003) A novel Antarctic microbial endolithic community within gypsum crusts. Environ Microbiol 5:555–565
Johnston CG, Vestal JR (1989) Distribution of inorganic species in two Antarctic cryptoendolithic microbial communities. Geomicrobiol J 7:137–153
Kappen L, Friedmann E, Garty J (1983) Ecophysiology of lichens in the Dry Valleys of Southern Victoria Land, Antarctica. Polar Biol 1:227–232
Khan N, Tuffin M, Stafford W, Cary C, Lacap DC, Pointing SB (2011) Hypolithic microbial communities of quartz rocks from Miers Valley, McMurdo Dry Valleys, Antarctica. Polar Biol 34:1657–1668
Lacap DC, Warren-Rhodes KA, McKay CP, Pointing SB (2010) Cyanobacteria and Chloroflexi-dominated hypolithic colonization of quartz at the hyper-arid core of the Atacama Desert, Chile. Extremophiles 15:31–38
Makhalanyane TP, Valverde A, Birkeland NK, Cary SC, Marla Tuffin I, Cowan DA (2013a) Evidence for successional development in Antarctic hypolithic bacterial communities. ISME J 7 2080–2090. doi:10.1038/ismej.2013.94
Makhalanyane TP, Valverde A, Lacap DC, Pointing SB, Tuffin MI, Cowan DA (2013b) Evidence of species recruitment and development of hot desert hypolithic communities. Environ Microbiol Rep 5:219–224
McKay CP, Friedmann EI (1985) The cryptoendolithic microbial environment in the Antarctic Cold Desert: temperature variations in nature. Polar Biol 4:19–25
McKay CP, Friedmann EI, Gómez-Silva B, Cáceres-Villanueva L, Andersen DT, Landheim R (2003) Temperature and moisture conditions for life in the extreme arid region of the Atacama Desert: four years of observations including the El Niño of 1997–1998. Astrobiology 3:393–406
McKnight MW, White PS, McDonald RI, Lamoreux JF, Sechrest W, Ridgely RS (2007) Putting beta-diversity on the map: broad-scale congruence and coincidence in the extremes. PLoS Biol 5:2424–2432
Nash T, White S, Marsh J (1977) Lichen and moss distribution and biomass in hot desert ecosystems. Bryologist 80:470–479
Nienow JA, Friedmann EI (1993) Terrestrial lithophytic (rock) communities. Antarct microbiol 11:343–412
Nienow J, McKay C, Friedmann EI (1988) The cryptoendolithic microbial environment in the Ross Desert of Antarctica: light in the photosynthetically active region. Microbiol Ecol 16:271–289
Nienow J, Friedmann E, Ocampo‐Friedmann R (2003) Endolithic microorganisms in arid regions. doi:10.1002/0471263397.env267
Omelon CR (2008) Endolithic microbial communities in Polar Desert habitats. Geomicrobiol J 25:404–414
Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10:551–562
Pointing SB, Warren-Rhodes KA, Lacap DC, Rhodes KL, McKay CP (2007) Hypolithic community shifts occur as a result of liquid water availability along environmental gradients in China’s hot and cold hyperarid deserts. Environ Microbiol 9:414–424
Pointing SB, Chan Y, Lacap DC, Lau MC, Jurgens JA, Farrell RL (2009) Highly specialized microbial diversity in hyper-arid Polar Desert. Proc Natl Acad Sci USA 106:19964–19969
Schlesinger WH, Pippen JS, Wallenstein MD, Hofmockel KS, Klepeis DM, Mahall BE (2003) Community composition and photosynthesis by photoautotrophs under quartz pebbles, Southern Mojave Desert. Ecology 84:3222–3231
Smith AJE (1982) Epiphytes and Epiliths. In: Smith AJE (ed) Bryophyte Ecology. Springer, Netherlands, pp 191–227
Smith MC, Bowman JP, Scott FJ, Line MA (2000) Sublithic bacteria associated with Antarctic quartz stones. Antarct Sci 12:177–184
Smith JJ, Tow LA, Stafford W, Cary C, Cowan DA (2006) Bacterial diversity in three different Antarctic Cold Desert mineral soils. Microbiol Ecol 51:413–421
Šperl J, Trčková J (2008) Permeability and porosity of rocks and their relationship based on laboratory testing. Acta Geodyn Geomater 5:149
Staley JT, Palmer F, Adams JB (1982) Microcolonial fungi: common inhabitants on desert rocks? Science 215:1093–1095
Stomeo F, Valverde A, Pointing SB, McKay CP, Warren-Rhodes KA, Tuffin MI, Seely M, Cowan DA (2013) Hypolithic and soil microbial community assembly along an aridity gradient in the Namib Desert. Extremophiles 17:329–337
Sun HJ, Friedmann EI (1999) Growth on geological time scales in the Antarctic cryptoendolithic microbial community. Geomicrobiol J 16:193–202
Sun H, Nienow J, McKay C (2010) Antarct cryptoendolithic microbial ecosystems. Life in Antarctic Deserts cold dry environments astrobiological analogs. Cambridge University Press, Cambridge, p 307
Thomas DS (1997) Arid environments: their nature and extent. In: Thomas DS (ed) Arid Zone Geomorphology: Process, Form and Change in Drylands, 3rd edn, pp 1–16.
Tracy CR, Streten-Joyce C, Dalton R, Nussear KE, Gibb KS, Christian KA (2010) Microclimate and limits to photosynthesis in a diverse community of hypolithic cyanobacteria in northern Australia. Environ Microbiol 12:592–607
Vincent WF (2004) Microbial ecosystems of Antarct. University of Cambridge, Cambridge, p 320
Warren-Rhodes KA, Rhodes KL, Pointing SB, Ewing SA, Lacap DC, Gomez-Silva B, Amundson R, Friedmann EI, McKay CP (2006) Hypolithic cyanobacteria, dry limit of photosynthesis, and microbial ecology in the hyperarid Atacama Desert. Microbiol Ecol 52:389–398
Warren-Rhodes KA, Rhodes KL, Boyle LN, Pointing SB, Chen Y, Liu S, Zhuo P, McKay CP (2007) Cyanobacterial ecology across environmental gradients and spatial scales in China’s hot and cold deserts. FEMS Microbiol Ecol 61:470–482
Wierzchos J, Ascaso C, McKay CP (2006) Endolithic cyanobacteria in halite rocks from the hyperarid core of the Atacama Desert. Astrobiology 6:415–422
Wong FK, Lacap DC, Lau MC, Aitchison JC, Cowan DA, Pointing SB (2010a) Hypolithic microbial community of quartz pavement in the high–altitude tundra of central Tibet. Microbiol Ecol 60:730–739
Wong FK, Lau MC, Lacap DC, Aitchison JC, Cowan DA, Pointing SB (2010b) Endolithic microbial colonization of limestone in a high–altitude arid environment. Microbiol Ecol 59:689–699
Wood SA, Rueckert A, Cowan DA, Cary SC (2008) Sources of edaphic cyanobacterial diversity in the Dry Valleys of Eastern Antarctica. ISME J 2:308–320
Wynn-Williams D (2002) Cyanobacteria in deserts—life at the limit? In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Kluwer Academic Publishers, Boca Raton, pp 341–366
Wynn-Williams D, Edwards H (2000) Antarctic ecosystems as models for extraterrestrial surface habitats. Planet Space Sci 48:1065–1075
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Makhalanyane, T.P., Pointing, S.B., Cowan, D.A. (2014). Lithobionts: Cryptic and Refuge Niches. In: Cowan, D. (eds) Antarctic Terrestrial Microbiology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-45213-0_9
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