Draft Metagenomes of Endolithic Cyanobacteria and Cohabitants from Hyper-Arid Deserts.
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ABSTRACT:
SUBMITTER: Murray B
PROVIDER: S-EPMC8320458 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:In hyper-arid deserts, endolithic microbial communities survive in the pore spaces and cracks of rocks, an environment that enhances water retention and filters UV radiation. The rock colonization zone is enriched in far-red light (FRL) and depleted in visible light. This poses a challenge to cyanobacteria, which are the primary producers of endolithic communities. Many species of cyanobacteria are capable of Far-Red-Light Photoacclimation (FaRLiP), a process in which FRL induces the synthesis of specialized chlorophylls and remodeling of the photosynthetic apparatus, providing the ability to grow in FRL. While FaRLiP has been reported in cyanobacteria from various low-light environments, our understanding of light adaptations for endolithic cyanobacteria remains limited. Here, we demonstrated that endolithic Chroococcidiopsis isolates from deserts around the world synthesize chlorophyll f, an FRL-specialized chlorophyll when FRL is the sole light source. The metagenome-assembled genomes of these isolates encoded chlorophyll f synthase and all the genes required to implement the FaRLiP response. We also present evidence of FRL-induced changes to the major light-harvesting complexes of a Chroococcidiopsis isolate. These findings indicate that endolithic cyanobacteria from hyper-arid deserts use FRL photoacclimation as an adaptation to the unique light transmission spectrum of their rocky habitat.
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Project description:Under extreme water deficit, endolithic (inside rock) microbial ecosystems are considered environmental refuges for life in cold and hot deserts, yet their diversity and functional adaptations remain vastly unexplored. The metagenomic analyses of the communities from two rock substrates, calcite and ignimbrite, revealed that they were dominated by Cyanobacteria, Actinobacteria, and Chloroflexi. The relative distribution of major phyla was significantly different between the two substrates and biodiversity estimates, from 16S rRNA gene sequences and from the metagenomic data, all pointed to a higher taxonomic diversity in the calcite community. While both endolithic communities showed adaptations to extreme aridity and to the rock habitat, their functional capabilities revealed significant differences. ABC transporters and pathways for osmoregulation were more diverse in the calcite chasmoendolithic community. In contrast, the ignimbrite cryptoendolithic community was enriched in pathways for secondary metabolites, such as non-ribosomal peptides (NRP) and polyketides (PK). Assemblies of the metagenome data produced population genomes for the major phyla found in both communities and revealed a greater diversity of Cyanobacteria population genomes for the calcite substrate. Draft genomes of the dominant Cyanobacteria in each community were constructed with more than 93% estimated completeness. The two annotated proteomes shared 64% amino acid identity and a significantly higher number of genes involved in iron update, and NRPS gene clusters, were found in the draft genomes from the ignimbrite. Both the community-wide and genome-specific differences may be related to higher water availability and the colonization of large fissures and cracks in the calcite in contrast to a harsh competition for colonization space and nutrient resources in the narrow pores of the ignimbrite. Together, these results indicated that the habitable architecture of both lithic substrates- chasmoendolithic versus cryptoendolithic - might be an essential element in determining the colonization and the diversity of the microbial communities in endolithic substrates at the dry limit for life.
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Project description:The adaptation mechanisms of microbial communities to natural perturbations remain unexplored, particularly in extreme environments. The extremophilic communities of halite (NaCl) nodules from the hyper-arid core of the Atacama Desert are self-sustained and represent a unique opportunity to study functional adaptations and community dynamics with changing environmental conditions. We transplanted halite nodules to different sites in the desert and investigated how their taxonomic, cellular, and biochemical changes correlated with water availability, using environmental data modeling and metagenomic analyses. Salt-in strategists, mainly represented by haloarchaea, significantly increased in relative abundance at sites characterized by extreme dryness, multiple wet/dry cycles, and colder conditions. The functional analysis of metagenome-assembled genomes (MAGs) revealed site-specific enrichments in archaeal MAGs encoding for the uptake of various compatible solutes and for glycerol utilization. These findings suggest that opportunistic salt-in strategists took over the halite communities at the driest sites. They most likely benefited from compounds newly released in the environment by the death of microorganisms least adapted to the new conditions. The observed changes were consistent with the need to maximize cellular bioenergetics when confronted with lower water availability and higher salinity, providing valuable information on microbial community adaptations and resilience to climate change.
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Project description:Studies of microbial biogeography are often convoluted by extremely high diversity and differences in microenvironmental factors such as pH and nutrient availability. Desert endolithic (inside rock) communities are relatively simple ecosystems that can serve as a tractable model for investigating long-range biogeographic effects on microbial communities. We conducted a comprehensive survey of endolithic sandstones using high-throughput marker gene sequencing to characterize global patterns of diversity in endolithic microbial communities. We also tested a range of abiotic variables in order to investigate the factors that drive community assembly at various trophic levels. Macroclimate was found to be the primary driver of endolithic community composition, with the most striking difference witnessed between hot and polar deserts. This difference was largely attributable to the specialization of prokaryotic and eukaryotic primary producers to different climate conditions. On a regional scale, microclimate and properties of the rock substrate were found to influence community assembly, although to a lesser degree than global hot versus polar conditions. We found new evidence that the factors driving endolithic community assembly differ between trophic levels. While phototrophic taxa, mostly oxygenic photosynthesizers, were rigorously selected for among different sites, heterotrophic taxa were more cosmopolitan, suggesting that stochasticity plays a larger role in heterotroph assembly. This study is the first to uncover the global drivers of desert endolithic diversity using high-throughput sequencing. We demonstrate that phototrophs and heterotrophs in the endolithic community assemble under different stochastic and deterministic influences, emphasizing the need for studies of microorganisms in context of their functional niche in the community.
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Project description:Quartz stones are ubiquitous in deserts and are a substrate for hypoliths, microbial colonists of the underside of such stones. These hypoliths thrive where extreme temperature and moisture stress limit the occurrence of higher plant and animal life. Several studies have reported the occurrence of green hypolithic colonization dominated by cyanobacteria. Here, we describe a novel red hypolithic colonization from Yungay, at the hyper-arid core of the Atacama Desert in Chile. Comparative analysis of green and red hypoliths from this site revealed markedly different microbial community structure as revealed by 16S rRNA gene clone libraries. Green hypoliths were dominated by cyanobacteria (Chroococcidiopsis and Nostocales phylotypes), whilst the red hypolith was dominated by a taxonomically diverse group of chloroflexi. Heterotrophic phylotypes common to all hypoliths were affiliated largely to desiccation-tolerant taxa within the Actinobacteria and Deinococci. Alphaproteobacterial phylotypes that affiliated with nitrogen-fixing taxa were unique to green hypoliths, whilst Gemmatimonadetes phylotypes occurred only on red hypolithon. Other heterotrophic phyla recovered with very low frequency were assumed to represent functionally relatively unimportant taxa.
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Project description:It is often difficult to decide which cyanobacteria found in endolithic habitats of calcite spring-tufa deposits are present as ephemeral components of the biota or are persistent, structural elements. To answer this question, we repeatedly studied two microhabitats of contrasting calcareous tufa springs in the European Alps. Pigment extracts, fluorescence probe measurements of in situ samples and traditional microscopy confirmed the dominance of cyanobacteria over eukaryotic algae and their viability in both microhabitats. Spring Site 1 (Laas, Northern Italy) is characterized by a highly variable, moist to dry and sun-exposed waterfall tufa consisting of fibrous calcite. A segment of these deposits in the lateral flank of a grotto contained dark endolithic layers in dim light, 1-2 mm below the surface, where aggregated cyanobacterial cells were dominant but not directly attached to calcites, a potential sign of gentle endolithic dissolution rather than calcite precipitation induced by cyanobacteria. Site 2 (Mühlau, Austria), in contrast, is a moss-tufa microhabitat associated with a seepage spring situated in a shady gorge, where the targeted stromatolites consisted of bark-like sheets of friable, orange to light-brown when wet (drying violet) 'styrofoam'- like aggregates of minute crystallites on the day-light exposed surfaces. These calcites were observed to nucleate directly on external sheaths of viable cyanobacteria trichomes. A polyphasic approach including LM, SEM, TEM exhibited a number of identical but also some divergent cyanobacteria of which two key taxa were specific for each of the two microhabitats (Nostoc and Pseudoscytonema at Sites 1 and 2 respectively). Both cyanobacterial communities characterised, by the cloning of 16S rDNA showed a dominance of mostly unknown and partly divergent filamentous cyanobacteria assigned to the order of Synechococcales. Our microhabitat study of alpine crenal calcites highlights the rather divergent biotic responses of cyanobacteria within spring tufa deposits.
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Project description: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.
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Project description:Toxic metabolites are produced by many cyanobacterial species. There are limited data on toxigenic benthic, mat-forming cyanobacteria, and information on toxic cyanobacteria from Central Asia is even more scarce. In the present study, we examined cyanobacterial diversity and community structure, the presence of genes involved in toxin production and the occurrence of cyanotoxins in cyanobacterial mats from small water bodies in a cold high-mountain desert of Eastern Pamir. Diversity was explored using amplicon-based sequencing targeting the V3-V4 region of the 16S rRNA gene, toxin potential using PCR-based methods (mcy, nda, ana, sxt), and toxins by enzyme-linked immunosorbent assays (ELISAs) and liquid chromatography-tandem mass spectrometry (LC-MS/MS). Molecular identification of cyanobacteria showed a high similarity of abundant taxa to Nostoc PCC-73102, Nostoc PCC-7524, Nodularia PCC-935 and Leptolyngbya CYN68. The PCRs revealed the presence of mcyE and/or ndaF genes in 11 samples and mcyD in six. The partial sequences of the mcyE gene showed high sequence similarity to Nostoc, Planktothrix and uncultured cyanobacteria. LC-MS/MS analysis identified six microcystin congeners in two samples and unknown peptides in one. These results suggest that, in this extreme environment, cyanobacteria do not commonly produce microcystins, anatoxins and cylindrospermopsins, despite the high diversity and widespread occurrence of potentially toxic taxa.
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