Antarctolichenia onofrii gen. nov. sp. nov. from Antarctic Endolithic Communities Untangles the Evolution of Rock-Inhabiting and Lichenized Fungi in Arthoniomycetes

Microbial endolithic communities are the main and most widespread life forms in the coldest and hyper-arid desert of the McMurdo Dry Valleys and other ice-free areas across Victoria Land, Antarctica. There, the lichen-dominated communities are complex and self-supporting assemblages of phototrophic and heterotrophic microorganisms, including bacteria, chlorophytes, and both free-living and lichen-forming fungi living at the edge of their physiological adaptability. In particular, among the free-living fungi, microcolonial, melanized, and anamorphic species are highly recurrent, while a few species were sometimes found to be associated with algae. One of these fungi is of paramount importance for its peculiar traits, i.e., a yeast-like habitus, co-growing with algae and being difficult to propagate in pure culture. In the present study, this taxon is herein described as the new genus Antarctolichenia and its type species is A. onofrii, which represents a transitional group between the free-living and symbiotic lifestyle in Arthoniomycetes. The phylogenetic placement of Antarctolichenia was studied using three rDNA molecular markers and morphological characters were described. In this study, we also reappraise the evolution and the connections linking the lichen-forming and rock-inhabiting lifestyles in the basal lineages of Arthoniomycetes (i.e., Lichenostigmatales) and Dothideomycetes.

Rock traits drive complex microbial communities at the edge of life

Antarctic deserts are among the driest and coldest ecosystems of the planet; there, some microbes hang on to life under these extreme conditions inside porous rocks, forming the so-called endolithic communities. Yet, the contribution of distinct rock traits to support complex microbial assemblies remains poorly determined. Here, we combined an extensive Antarctic rock survey with rock microbiome sequencing and ecological networks, and found that contrasting combinations of microclimatic and rock traits such as thermal inertia, porosity, iron concentration and quartz cement can help explain the multiple complex and independent microbial assemblies found in Antarctic rocks. Our work highlights the pivotal role of rocky substrate heterogeneity in sustaining contrasting groups of microorganisms, which is essential to understand life at the edge on Earth, and for searching life on other rocky planets such as Mars.

Connectivity of Edaphic and Endolithic Microbial Niches in Cold Mountain Desert of Eastern Pamir (Tajikistan)

Microbial communities found in arid environments are commonly represented by biological soil crusts (BSCs) and endolithic assemblages. There is still limited knowledge concerning endoliths and BSCs occurring in the cold mountain desert of Pamir. The aim of the study was to investigate the composition and structure of endolithic bacterial communities in comparison to surrounding BSCs in three subregions of the Eastern Pamir (Tajikistan). The endolithic and BSC communities were studied using culture-independent and culture-dependent techniques. The structure of the endolithic bacterial communities can be characterized as Actinobacteria–Proteobacteria–Bacteroidetes–Chloroflexi–Cyanobacteria, while the BSCs’ can be described as Proteobacteria–Actinobacteria–Bacteroidetes–Cyanobacteria assemblages with low representation of other bacteria. The endolithic cyanobacterial communities were characterized by the high percentage of Chroococcidiopsaceae, Nodosilineaceae, Nostocaceae and Thermosynechococcaceae, while in the BSCs were dominated by Nodosilineaceae, Phormidiaceae and Nostocaceae. The analysis of 16S rRNA genes of the cyanobacterial cultures revealed the presence of possibly novel species of Chroococcidiopsis, Gloeocapsopsis and Wilmottia. Despite the niches’ specificity, which is related to the influence of microenvironment factors on the composition and structure of endolithic communities, our results illustrate the interrelation between the endoliths and the surrounding BSCs in some regions. The structure of cyanobacterial communities from BSC was the only one to demonstrate some subregional differences.

The composition of endolithic communities in gypcrete is determined by the specific microhabitat architecture

Endolithic microhabitats have been described as the last refuge for life in arid and hyper-arid deserts where life has to deal with harsh environmental conditions. A number of rock substrates from the hyper-arid Atacama Desert, colonized by endolithic microbial communities such as halite, gypsum crusts, gypcrete, calcite, granite and ignimbrite, have been characterized and compared using different approaches. In this work, three different endolithic microhabitats are described, each one with a particular origin and architecture, found within a lithic substrate known as gypcrete. Gypcrete, an evaporitic rock mainly composed of gypsum (CaSO4 ⋅ 2H2O) and collected in the Cordón de Lila area of the desert (Preandean Atacama Desert), was found to harbour cryptoendolithic (within pore spaces in the rock), chasmoendolithic (within cracks and fissures) and hypoendolithic (within microcave-like pores in the bottom layer of rock) microhabitats. A combination of microscopy investigation and high-throughput sequencing approaches were used to characterize the endolithic communities and their habitats at the microscale within the same piece of gypcrete. Microscopy techniques revealed differences in the architecture of the endolithic microhabitats and the distribution of the microorganisms within those microhabitats. Cyanobacteria and Proteobacteria were dominant in the endolithic communities, of which the hypoendolithic community was the least diverse and hosted unique taxa, as a result of less access to sun radiation. These results show, for the first time, that the differences in the architecture of a microhabitat, even within the same piece of a lithic substrate, play an essential role in shaping the diversity and composition of endolithic microbial communities.

Metabolomics of Dry Versus Reanimated Antarctic Lichen-Dominated Endolithic Communities

Cryptoendolithic communities are almost the sole life form in the ice-free areas of the Antarctic desert, encompassing among the most extreme-tolerant organisms known on Earth that still assure ecosystems functioning, regulating nutrient and biogeochemical cycles under conditions accounted as incompatible with active life. If high-throughput sequencing based studies are unravelling prokaryotic and eukaryotic diversity, they are not yet characterized in terms of stress adaptations and responses, despite their paramount ecological importance. In this study, we compared the responses of Antarctic endolithic communities, with special focus on fungi, both under dry conditions (i.e., when dormant), and after reanimation by wetting, light, and optimal temperature (15 °C). We found that several metabolites were differently expressed in reanimated opposite sun exposed communities, suggesting a critical role in their success. In particular, the saccharopine pathway was up-regulated in the north surface, while the spermine/spermidine pathway was significantly down-regulated in the shaded exposed communities. The carnitine-dependent pathway is up-regulated in south-exposed reanimated samples, indicating the preferential involvement of the B-oxidation for the functioning of TCA cycle. The role of these metabolites in the performance of the communities is discussed herein.

Diversity and Colonization Strategies of Endolithic Cyanobacteria in the Cold Mountain Desert of Pamir

Microorganisms can survive in extreme environments and oligotrophic habitats thanks to their specific adaptive capacity. Due to its severe and contrasting climate conditions, the cold mountain desert in Eastern Pamir provides a unique environment for analyzing microbial adaptation mechanisms occurring within colonization of endolithic habitats. This study aims to investigate the composition and structure of endolithic microbial communities and analyze the interactions between microorganisms and colonized lithic substrates. Endolithic biofilms were examined using scanning electron microscopy in backscattered electron mode (SEM-BSE) and next-generation sequencing (NGS) applying amplicon sequence variants (ASVs) approach. The investigation of the V3–V4 region of 16S rRNA gene revealed that endolithic communities are dominated by Actinobacteria (26%), Proteobacteria (23%), and Cyanobacteria (11.4%). Cyanobacteria were represented by Oxyphotobacteria with a predominance of subclasses of Oscillatoriophycidae, Synechococcophycideae, and Nostocophycidae as well as the rarely occurring Sericytochromatia. The positive correlation between the contribution of the orders Synechococcales and Rhizobiales to community structure suggests that some functionally closed taxa of Cyanobacteria and Proteobacteria can complement each other, for example, in nitrogen fixation in endolithic communities. The endolithic communities occurring in Eastern Pamir were identified as complex systems whose composition and structure seem to be influenced by the architecture of microhabitats and related microenvironmental conditions.

Effects of Ocean Acidification on Coral Endolithic Bacterial Communities in Isopora palifera and Porites lobata

Endolithic microbes in coral reefs may act as a nutrient source for their coral hosts. Increasing atmospheric CO2 concentrations are causing ocean acidification (OA), which may affect marine organisms and ecosystems, especially calcifying organisms such as reef-building corals. However, knowledge of how OA affects marine microbes remains limited, and little research has been done on how coral endolithic communities respond to shifting environmental baselines. In this study, the endolithic communities of two common shallow water coral species, Isopora palifera and Porites lobata, were examined to investigate the microbial community dynamics under OA treatments. The colonies were placed in an environment with a partial pressure of carbon dioxide (pCO2) of 1,000 or 400 ppm (control) for 2 months. Several I. palifera colonies bleached and died at 1,000 ppm pCO2, but the P. lobata colonies remained unaffected. Inversely, the endolithic community in P. lobata skeletons showed significant changes after OA treatment, whereas no significant dynamics were observed among the I. palifera endoliths. Our findings suggest that the skeletal structures of different coral species may play a key role in corals host and endoliths under future high-OA scenarios.

The composition of endolithic communities in gypcrete is determined by the specific microhabitat architecture

Endolithic microhabitats have been described as the last refuge for life in arid and hyper-arid deserts where life has to deal with harsh environmental conditions. A number of rock substrates from the hyper-arid Atacama Desert, colonized by endolithic microbial communities, such as halite, gypsum crusts, gypcrete, calcite, granite and ignimbrite, have been characterized and compared using different approaches. In this work, three different endolithic microhabitats are described, each one with a particular origin and architecture, found within a lithic substrate known as gypcrete. Gypcrete, an evaporitic rock mainly composed of gypsum (CaSO4 ⋅ 2H2O) and collected in the Cordón de Lila area of the desert (Preandean Atacama Desert), was found to harbour cryptoendolithic (within pore spaces in the rock), chasmoendolithic (within cracks and fissures) and hypoendolithic (within microcave-like pores in rock-bottom layer) microhabitats. A combination of microscopy investigations strategies and high-throughput sequencing approaches were used to characterize the endolithic communities at the microscale in these microhabitats within the same piece of lithic substrate. Microscopy techniques revealed differences in the architecture of the endolithic microhabitats and in the distribution of the microorganisms within those microhabitats. Cyanobacteria and Proteobacteria were dominant in the endolithic communities, of which the hypoendolithic community was the least diverse and hosted unique taxa. These results show, for the first time, that the differences in the architecture of a microhabitat, even within the same piece of lithic substrate, might be an essential factor in shaping the diversity and composition of endolithic microbial communities.

Biogeomorphology at the micro-scale: biogeochemical weathering of rock surfaces in the cold and warm deserts

<p><span>Biogeochemical weathering of stable rock surfaces in warm and cold deserts is a notable biogeomorphological process, which contribute to mineralogical transformation of rock constituents and rock disaggregation. Endolithic microorganisms (mostly bacteria, fungi and lichens) play a major role in controlling the destabilization and rejunevation of rock surfaces; but occasionally, biofilms can stabilize rock surfaces. In most of the casis, endolithic communities precipitates byproducts (e.g. oxalates) contributing to enhance discotnituity and promoting exfoliation and disaggregation. On the contrary, rock varnish can develop as an external crust protecting the underliyng rock from erosion and dissolution. In this contribution, a number of case-studies of fossil and active examples of biogeochemical weathering from warm deserts of Africa and Arabian peninsula and from Antarctica are considered. The comaprison of evidence suggests a highly differentiate –  and occasioanlly surprisingly – array of effects of endolithic communities on rock surfaces.</span></p>