Cyanobacteria and chloroflexi-dominated hypolithic colonization of quartz at the hyper-arid core of the Atacama Desert,Chile

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.     

Water availability shapes edaphic and lithic cyanobacterial communities in the Atacama Desert

In the Atacama Desert, cyanobacteria grow on various substrates such as soils (edaphic) and quartz or granitoid stones (lithic). Both edaphic and lithic cyanobacterial communities have been described but no comparison between both communities of the same locality has yet been undertaken. In the present study, we compared both cyanobacterial communities along a precipitation gradient ranging from the arid National Park Pan de Azúcar (PA), which resembles a large fog oasis in the Atacama Desert extending to the semiarid Santa Gracia Natural Reserve (SG) further south, as well as along a precipitation gradient within PA. Various microscopic techniques, as well as culturing and partial 16S rRNA sequencing, were applied to identify 21 cyanobacterial species; the diversity was found to decline as precipitation levels decreased. Additionally, under increasing xeric stress, lithic community species composition showed higher divergence from the surrounding edaphic community, resulting in indigenous hypolithic and chasmoendolithic cyanobacterial communities. We conclude that rain and fog water, respectively, cause contrasting trends regarding cyanobacterial species richness in the edaphic and lithic microhabitats.     

Hypolithic Cyanobacteria, Dry Limit of Photosynthesis, and Microbial Ecology in the Hyperarid Atacama Desert

The occurrence of hypolithic cyanobacteria colonizing translucent stones was quantified along the aridity gradient in the Atacama Desert in Chile, from less arid areas to the hyperarid core where photosynthetic life and thus primary production reach their limits. As mean rainfall declines from 21 to ≤2 mm year⁻¹, the abundance of hypolithic cyanobacteria drops from 28 to <0.1%, molecular diversity declines threefold, and organic carbon residence times increase by three orders of magnitude. Communities contained a single Chroococcidiopsis morphospecies with heterotrophic associates, yet molecular analysis revealed that each stone supported a number of unique 16S rRNA gene-defined genotypes. A fivefold increase in steady-state residence times for organic carbon within communities in the hyperarid core (3200 years turnover time) indicates a significant decline in biological carbon cycling. Six years of microclimate data suggest that the dry limit corresponds to ≤5 mm year⁻¹ rainfall and/or decadal periods of no rain, with <75 h year⁻¹ of liquid water available to cyanobacteria under light conditions suitable for photosynthesis. In the hyperarid core, hypolithic cyanobacteria are rare and exist in small spatially isolated islands amidst a microbially depauperate bare soil. These findings suggest that photosynthetic life is extremely unlikely on the present-day surface of Mars, but may have existed in the past. If so, such microhabitats would probably be widely dispersed, difficult to detect, and millimeters away from virtually lifeless surroundings.     

Hypolithic Cyanobacteria Supported Mainly by Fog in the Coastal Range of the Atacama Desert

The Atacama Desert is one of the driest places on Earth, with an arid core highly adverse to the development of hypolithic cyanobacteria. Previous work has shown that when rain levels fall below ~1 mm per year, colonization of suitable quartz stones falls to virtually zero. Here, we report that along the coast in these arid regions, complex associations of cyanobacteria, archaea, and heterotrophic bacteria inhabit the undersides of translucent quartz stones. Colonization rates in these areas, which receive virtually no rain but mainly fog, are significantly higher than those reported inland in the hyperarid zone at the same latitude. Here, hypolithic colonization rates can be up to 80%, with all quartz rocks over 20 g being colonized. This finding strongly suggests that hypolithic microbial communities thriving in the seaward face of the Coastal Range can survive with fog as the main regular source of moisture. A model is advanced where the development of the hypolithic communities under quartz stones relies on a positive feedback between fog availability and the higher thermal conductivity of the quartz rocks, which results in lower daytime temperatures at the quartz–soil interface microenvironment.     

Sub-lithic photosynthesis in hot desert habitats

In hyper-arid soil environments, photosynthetic microorganisms are largely restricted to hypolithic (sub-lithic) habitats: i.e., on the ventral surfaces of translucent pebbles in desert pavements. Here, we combined fluorometric, spectroscopic, biochemical and metagenomic approaches to investigate in situ the light transmission properties of quartz stones in the Namib Desert, and assess the photosynthetic activity of the underlying hypolithic cyanobacterial biofilms. Quartz pebbles greatly reduced the total photon flux to the ventral surface biofilms and filtered out primarily the short wavelength portion of the solar spectrum. Chlorophylls d and f were not detected in biofilm pigment extracts; however, hypolithic cyanobacterial communities showed some evidence of adaptation to sub-lithic conditions, including the prevalence of genes encoding Helical Carotenoid Proteins, which are associated with desiccation stress. Under water-saturated conditions, hypolithic communities showed no evidence of light stress, even when the quartz stones were exposed to full midday sunlight. This initial study creates a foundation for future in-situ and laboratory exploration of various adaptation mechanisms employed by photosynthetic organisms forming hypolithic microbial communities.     

Microclimate and limits to photosynthesis in a diverse community of hypolithic cyanobacteria in northern Australia

Hypolithic microbes, primarily cyanobacteria, inhabit the highly specialized microhabitats under translucent rocks in extreme environments. Here we report findings from hypolithic cyanobacteria found under three types of translucent rocks (quartz, prehnite, agate) in a semiarid region of tropical Australia. We investigated the photosynthetic responses of the cyanobacterial communities to light, temperature and moisture in the laboratory, and we measured the microclimatic variables of temperature and soil moisture under rocks in the field over an annual cycle. We also used molecular techniques to explore the diversity of hypolithic cyanobacteria in this community and their phylogenetic relationships within the context of hypolithic cyanobacteria from other continents. Based on the laboratory experiments, photosynthetic activity required a minimum soil moisture of 15% (by mass). Peak photosynthetic activity occurred between approximately 8°C and 42°C, though some photosynthesis occurred between ?1°C and 51°C. Maximum photosynthesis rates also occurred at light levels of approximately 150–550 μmol m^?2 s^?1. We used the field microclimatic data in conjunction with these measurements of photosynthetic efficiency to estimate the amount of time the hypolithic cyanobacteria could be photosynthetically active in the field. Based on these data, we estimated that conditions were appropriate for photosynthetic activity for approximately 942 h (～75 days) during the year. The hypolithic cyanobacteria community under quartz, prehnite and agate rocks was quite diverse both within and between rock types. We identified 115 operational taxonomic units (OTUs), with each rock hosting 8–24 OTUs. A third of the cyanobacteria OTUs from northern Australia grouped with Chroococcidiopsis, a genus that has been identified from hypolithic and endolithic communities from the Gobi, Mojave, Atacama and Antarctic deserts. Several OTUs identified from northern Australia have not been reported to be associated with hypolithic communities previously.     

Hypolithic microbial communities of quartz rocks from Miers Valley, McMurdo Dry Valleys, Antarctica

The McMurdo Dry Valleys region of eastern Antarctica is a cold desert that presents extreme challenges to life. Hypolithic microbial colonisation of the subsoil surfaces of translucent quartz rocks represent a significant source of terrestrial biomass and productivity in this region. Previous studies have described hypoliths as dominated by cyanobacteria. However, hypoliths that occur in the lower Dry Valleys such as the Miers, Garwood and Marshall Valleys are unusual as they are not necessarily cyanobacteria-dominated. These hypoliths support significant eukaryal colonisation by fungi and mosses in addition to cyanobacteria-dominated bacterial assemblages and so have considerable ecological value in this barren landscape. Here, we characterise these novel hypoliths by analysis of environmental rRNA gene sequences. The hypolithic community was demonstrated to be distinct from the surrounding soil and non-translucent rocks. Hypoliths supported cyanobacterial signatures from the Oscillatoriales and Nostocales. Other heterotrophic bacterial signatures were also recovered, and these were phylogenetically diverse and spanned 8 other bacterial phyla. Archaeal phylotypes recovered were phylogenetically affiliated with the large group of unclassified, uncultured Crenarcheota. Eukaryal phylotypes indicated that free-living ascomycetous fungi, chlorophytes and mosses (Bryum sp.) were all supported by these hypoliths, and these are thought to be responsible for the extensive eukaryotic biomass that develops around quartz rocks.     

JET‐SUSPENDED,CALCITE‐BALLASTED CYANOBACTERIAL WATERWARTS IN A DESERT SPRING1

We describe a population of colonial cyanobacteria (waterwarts) that develops as the dominant primary producer in a bottom‐fed, O₂‐poor, warm spring in the Cuatro Ciénegas karstic region of the Mexican Chihuahuan Desert. The centimeter‐sized waterwarts were suspended within a central, conically shaped, 6‐m deep well by upwelling waters. Waterwarts were built by an Aphanothece‐like unicellular cyanobacterium and supported a community of epiphytic filamentous cyanobacteria and diatoms but were free of heterotrophic bacteria inside. Sequence analysis of 16S rRNA genes revealed that this cyanobacterium is only distantly related to several strains of other unicellular cyanobacteria (Merismopedia, Cyanothece, Microcystis). Waterwarts contained orderly arrangements of mineral crystallites, made up of microcrystalline low‐magnesium calcite with high levels of strontium and sulfur. Waterwarts were 95.9% (v/v) glycan, 2.8% cells, and 1.3% mineral grains and had a buoyant density of 1.034 kg·L^?1. An analysis of the hydrological properties of the spring well and the waterwarts demonstrated that both large colony size and the presence of controlled amounts of mineral ballast are required to prevent the population from being washed out of the well. The unique hydrological characteristics of the spring have likely selected for both traits. The mechanisms by which controlled nucleation of extracellular calcite is achieved remain to be explored.     

Application of real-time PCR in the assessment of the toxic cyanobacterium <Emphasis Type="Italic">Cylindrospermopsis raciborskii</Emphasis> abundance and toxicological potential

Cyanobacteria are prokaryotic photosynthetic microorganisms that pose a serious threat to aquatic environments because they are able to form blooms under eutrophic conditions and produce toxins. Cylindrospermopsis raciborskii is a planktonic heterocystous filamentous cyanobacterium initially assigned to the tropics but currently being found in more temperate regions such as Portugal, the southernmost record for this species in Europe. Cylindrospermopsin originally isolated from C. raciborskii is a cytotoxic alkaloid that affects the liver, kidney, and other organs. It has a great environmental impact associated with cattle mortality and human morbidity. Aiming in monitoring this cyanobacterium and its related toxin, a shallow pond located in the littoral center of Portugal, Vela Lake, used for agriculture and recreational purposes was monitored for a 2-year period. To accomplish this, we used the real-time PCR methodology in field samples to quantify the variation of specific genetic markers with primers previously described characterizing total cyanobacteria (16S rRNA), C. raciborskii (rpoC1), and cylindrospermopsin synthetase gene (pks). The results report the high abundance of both cyanobacteria and C. raciborskii in Vela Lake, with C. raciborskii representing 0.4% to 58% of the total cyanobacteria population. Cylindrospermopsin synthetase gene was detected in one of the samples. We believe that with the approach developed in this study, it will be possible to monitor C. raciborskii population dynamics and seasonal variation, as well as the potential toxin production in other aquatic environments.     

基于克隆文库法研究古尔班通古特沙漠蓝藻多样性

该研究采用克隆文库法研究古尔班通古特沙漠藻类生物结皮中蓝藻多样性及分布。在古尔班通古特沙漠不同区域采集10份藻类结皮代表性土样,分别构建古尔班通古特沙漠蓝藻16S rRNA和psbA基因克隆文库,并进行系统发育分析,对蓝藻多样性和丰度与环境因子进行关联分析,研究蓝藻分布特点及影响因子。结果显示:(1)16S rRNA基因系统发育树中包括具有明确分类地位的蓝藻有6科10属(占总克隆文库的94.85%)和一个未分类蓝藻属,其中颤藻属(Oscillatoria)和微鞘藻属(Microcoleus)分别占克隆文库的42.54%和37.16%,为古尔班通古特沙漠蓝藻优势属;psbA基因系统发育树中仅鉴定有蓝藻类群4科4属,但优势属与前者结果一致。(2)10个样点藻类结皮中所含蓝藻种类不尽相同,但每个采样点都出现颤藻属和微鞘藻属,证明这二者是古尔班通古特沙漠藻类结皮中的优势属;且样点Gur2和Gur17中蓝藻种类较多,Gur3、Gur5和Gur9中种类较少,但Gur2、Gur3、Gur5和Gur17相对地理位置较近,表明地理位置不是影响蓝藻分布的主要因素。(3)RDA(Redundancy analysis)分析结果显示,微生物量氮(MBN)和土壤有机碳(SOC)对蓝藻多样性影响程度最大,其次是硝态氮(NO~-_3-N)、微生物量碳(MBC),全磷(TP)和全钾(TK)对其影响程度最小。研究表明,古尔班通古特沙漠不同区域沙漠蓝藻多样性和土壤理化性质具有空间异质性,综合分析可得沙漠中南部藻类结皮土壤营养最为丰富,蓝藻多样性较高,而东部和西部土壤营养较为贫瘠,蓝藻丰富度和多样性较低。     

Microbial colonization of the salt deposits in the driest place of the Atacama Desert (Chile)

The Atacama Desert (Chile), one of the most arid places on Earth, shows hostile conditions for the development of epilithic microbial communities. In this study, we report the association of cyanobacteria (Chroococcidiopsis sp.) and bacteria belonging to Actinobacteria and Beta-Gammaproteobacteria and Firmicutes phyla inhabiting the near surface of salt (halite) deposits of the Salar Grande Basin, Atacama Desert (Chile). The halite deposits were investigated by using optical, confocal and field emission scanning electron microscopes, whereas culture-independent molecular techniques, 16S rDNA clone library, alongside RFLP analysis and 16S rRNA gene sequencing were applied to investigate the bacterial diversity. These microbial communities are an example of life that has adapted to extreme environmental conditions caused by dryness, high irradiation, and metal concentrations. Their adaptation is, therefore, important in the investigation of the environmental conditions that might be expected for life outside of Earth.     

Fundamental drivers for endolithic microbial community assemblies in the hyperarid Atacama Desert

In hyperarid deserts, endolithic microbial communities colonize the rocks’ interior as a survival strategy. Yet, the composition of these communities and the drivers promoting their assembly are still poorly understood. We analysed the diversity and community composition of endoliths from four different lithic substrates – calcite, gypsum, ignimbrite and granite – collected in the hyperarid zone of the Atacama Desert, Chile. By combining microscopy, mineralogy, spectroscopy and high throughput sequencing, we found these communities to be highly specific to their lithic substrate, although they were all dominated by the same four main phyla, Cyanobacteria, Actinobacteria, Chloroflexi and Proteobacteria. Our finding indicates a fine scale diversification of the microbial reservoir driven by substrate properties. The data suggest that the overall rock chemistry and the light transmission properties of the substrates are not essential drivers of community structure and composition. Instead, we propose that the architecture of the rock, i.e., the space available for colonization and its physical structure, linked to water retention capabilities, is ultimately the driver of community diversity and composition at the dry limit of life.     

Acid microenvironments in microbial biofilms of antarctic endolithic microecosystems

Antarctic endolithic microecosystems harbour distinct biofilms. The lithic substrate and the microorganisms comprising these films are intimately linked, leading to complex mineral-microbe interactions. Hence, the microhabitats and microenvironments of these microecosystems are not only determined by the physicochemical features of the lithic substrate, but are also conditioned by the biological components of these biofilms. The Antarctic biofilms analysed in this study are characterized by the presence of extracellular polymer substances and acid microenvironments in the proximity of the cells; cyanobacteria appearing as key components. On ultrastructural analysis, these endolithic cyanobacteria showed differences in sheath organization, probably related to their spatial position in the lithic substrate. It is proposed that in this type of ecosystem, biofilm structure could favour the formation of microsites with specific physicochemical conditions appropriate for the survival of microbial communities in this extreme environment.     

Ancient Photosynthetic Eukaryote Biofilms in an Atacama Desert Coastal Cave

Caves offer a stable and protected environment from harsh and changing outside prevailing conditions. Hence, they represent an interesting habitat for studying life in extreme environments. Here, we report the presence of a member of the ancient eukaryote red algae Cyanidium group in a coastal cave of the hyperarid Atacama Desert. This microorganism was found to form a seemingly monospecific biofilm growing under extremely low photon flux levels. Our work suggests that this species, Cyanidium sp. Atacama, is a new member of a recently proposed novel monophyletic lineage of mesophilic “cave” Cyanidium sp., distinct from the remaining three other lineages which are all thermo-acidophilic. The cave described in this work may represent an evolutionary island for life in the midst of the Atacama Desert.     

Biological dinitrogen fixation by selected soil cyanobacteria as affected by strain origin,morphotype, and light conditions

The potential for N₂ fixation by heterocystous cyanobacteria isolated from soils of different geographical areas was determined as nitrogenase activity (NA) using the acetylene reduction assay. Morphology of cyanobacteria had the largest influence on NA determined under light conditions. NA was generally higher in species lacking thick slime sheaths. The highest value (1446 nmol/h C₂H₄ per g fresh biomass) was found in the strain of branched cyanobacterium Hassalia (A Has1) from the polar region. A quadratic relationship between NA and biomass was detected in the Tolypothrix group under light conditions. The decline of NA in dark relative to light conditions ranged from 37 to 100 % and differed among strains from distinct geographical areas. Unlike the NA of temperate and tropical strains, whose decline in dark relative to light was 24 and 17 %, respectively, the NA of polar strains declined to 1 % in the dark. This difference was explained by adaptation to different light conditions in temperate, tropical, and polar habitats. NA was not related to the frequency of heterocysts in strains of the colony-forming cyanobacterium Nostoc. Colony morphology and life cycle are therefore more important for NA then heterocyst frequency. NA values probably reflect the environmental conditions where the cyanobacterium was isolated and the physiological and morphological state of the strain.     

Biliproteins and phycobilisomes from cyanobacteria and red algae at the extremes of habitat

This review considers the properties of biliproteins from cyanobacteria and red algae that grow in extreme habitats. Three situations are presented: cyanobacteria that grow at high temperatures; a red alga that grows in acidic conditions at high temperature; and an Antarctic red alga that grows in the cold in dim light conditions. In particular, the properties of their biliproteins are compared to those from organisms from more usual environments. C-phycocyanins from two cyanobacteria able to grow at high temperatures are found to differ in their stabilities when compared to C-phycocyanin from mesophilic algae. They differ in opposite ways, however. One is more stable to dissociation than the mesophilic protein, and the other is more easily dissociated at low temperatures. The thermophilic proteins resist thermal denaturation much better than the mesophilic proteins. The most thermophilic cyanobacterium has a C-phycocyanin with a unique blue-shifted absorption maximum which does not appear to be part of the adaptation of the cyanobacterium to high temperature. The C-phycocyanin from the high-temperature red alga is able to resist dissociation better than mesophilic C-phycocyanins. Electron micrographs show the phycobilisomes of these algae. The Antarctic alga grows under ice at some distance down the water column. Its R-phycoerythrin has a novel absorption spectrum that gives the alga an improved ability to harvest blue light. This may enhance its survival in its light-deprived habitat.     

基于Illumina MiSeq测序技术的塔克拉玛干沙漠东缘细菌多样性分析

【背景】塔克拉玛干沙漠凭借其独特的地理位置、恶劣的生存环境以及较少的人为干扰,造就了其独特的微生物资源。【目的】探究塔克拉玛干沙漠东缘沙土细菌群落结构多样性及其影响因素。【方法】采集塔克拉玛干沙漠东缘沙土样品并测定其理化性质,使用基于原核微生物16S rRNA基因的IlluminaMiSeq测序技术,对塔克拉玛干沙漠东缘沙土进行细菌群落结构多样性及其影响因素的分析。【结果】从塔克拉玛干沙漠东缘沙土中获得明确分类地位的细菌种类为21门42纲304属,其中优势菌门为拟杆菌门(Bacteroidetes,31.26%)、变形菌门(Proteobacteria,29.47%)、放线菌门(Actinobacteria,15.71%)和厚壁菌门(Firmicutes,15.69%);在属水平上相对丰度最高的菌属为Salinimicrobium (10.06%),其次为盐单胞菌属(Halomonas,7.39%)、芽胞杆菌属(Bacillus,3.25%)、蓬托斯菌属(Pontibacter,3.14%)、Aliifodinibius(2.76%)和考克氏菌属(Kocuria,1.76%)。全磷(T...     

A diversity of bacteriophage forms and genomes can be isolated from the surface sands of the Sahara Desert

The surface sands of the Sahara Desert are exposed to extremes of ultraviolet light irradiation, desiccation and temperature variation. Nonetheless, the presence of bacteria has recently been demonstrated in this environment by cultivation methods and by 16S rDNA analyses from total DNA isolated from surface sands. To discern the presence of bacteriophages in this harsh environment, we searched for extracellular phages and intracellularly located phages present as prophages or within pseudolysogens. Mild sonication of the sand, in different liquid culture media, incubated with and without Mitomycin-C, was followed by differential centrifugation to enrich for dsDNA phages. The resulting preparations, examined by electron microscopy, revealed the presence of virus-like particles with a diversity of morphotypes representative of all three major double-stranded DNA bacteriophage families (Myoviridae, Siphoviridae and Podoviridae). Moreover, pulsed-field gel electrophoresis of DNA, extracted from the enriched bacteriophage preparations, revealed the presence of distinct bands suggesting the presence of putative dsDNA phage genomes ranging in size from 45 kb to 270 kb. Characterization of the bacteriophages present in the surface sands of the Sahara Desert extends the range of environments from which bacteriophages can be isolated, and provides an important point of departure for the study of phages in extreme terrestrial environments.Magali Prigent and Magali Leroy contributed equally to this work     

The spatial structures of hypolithic communities in the Dry Valleys of East Antarctica

Hypolithic communities represent important reservoirs of microbial life in hyper-arid deserts. A number of studies on the diversity and ecology of these communities from different geographic areas have been reported in the past decade, but the spatial distribution of the different components of these communities is still not understood. Moss- and cyanobacteria-dominated hypolithic community morphotypes from Miers Valley (McMurdo Dry Valleys, East Antarctica) were analyzed by electron microscopy in order to characterize the microscale spatial structure. The two communities showed a high degree of internal organization, but differing according to the biological composition. In moss-dominated hypoliths, the moss plantlets are intermixed with mineral fragments of soil origin. However, in cyanobacteria-dominated hypoliths, a layered spatial organization was structured by filamentous cyanobacteria and associated extracellular polymeric components. While moss cells were lacking in cyanobacteria-dominated communities, biofilms formed by cyanobacteria and heterotrophic bacteria were observed in both community morphotypes. The water-holding capacity of both live and dead moss cells and the associated organic matrix, together with the protective properties of the extracellular polymeric substances, could facilitate the survival and activity of these communities. Similar structural strategies can favor the survival of microbial communities in different extreme environments.