Errata corrige

Abstract

Ecological research on extreme environments can be applied to exobiological problems such as the question of life on Mars. If life forms (fossil or extant) are found on Mars, their study will help to solve fundamental questions about the nature of life on Earth. Extreme environments that are beyond the range of adaptability of their inhabitants are defined as “absolute extreme.” Such environments can serve as terrestrial models for the last stages of life in the history of Mars, when the surface cooled down and atmosphere and water disappeared. The cryptoendolithic microbial community in porous rocks of the Ross Desert in Antarctica and the microbial mats at the bottom of frozen Antarctic lakes are such examples. The microbial communities of Siberian permafrost show that, in frozen but stable communities, long-term survival is possible. In the context of terraforming Mars, selected microorganisms isolated from absolute extreme environments are considered for use in creation of a biological carbon cycle.     

What's up down there?

The development of careful quality assurance criteria assuring freedom from contamination in all aspects of sample recovery has opened the window to studies of a fascinating new microbial biome in the deep subsurface. Organisms have been recovered with unusual metabolic capabilities and a chemosynthetic lifestyle independent of the recent surface photosynthetically derived energy inputs. The properties of the subsurface microbiota are critical when assessing aspects such as the utility of burying radioactive waste, the remediation of mixtures of organics, metals, and nuclides, and the search for life in extreme environments on Earth as well as on Mars and other extraterrestrial sites. In addition this pioneering work provides a foundation for examining life processes in extreme environments, such as the environment beneath the ocean floor.     

Life on Mars

Abstract

There is evidence that at one time Mars had liquid water habitats on its surface. Studies of microbial communities in cold and dry environments on the Earth provide a basis for discussion of the possible nature of any life that may have existed on Mars during that time. Of particular relevance are the cyanobacterial communities found in hypolithic and endolithic habitats in deserts. Microbial mats found under ice-covered lakes provide an additional possible Martian system. Results obtained from these field studies can be used to guide the search for fossil evidence of life on Mars. It is possible that in the future life will be reintroduced on Mars in an effort to restore that planet to habitable conditions. In this case the organisms under study as exemplars of past life may provide the hardy stock of pioneering Martian organisms. These first organisms must be followed by plants. The feasibility of reviving Mars will depend on the ability of plants to grow in an abundance of CO₂ but at extremely low pressures, temperatures, O₂, and N₂ levels. On Mars, biology was, and is, destiny.     

An Unusual Inverted Saline Microbial Mat Community in an Interdune Sabkha in the Rub' al Khali (the Empty Quarter), United Arab Emirates

Salt flats (sabkha) are a recognized habitat for microbial life in desert environments and as analogs of habitats for possible life on Mars. Here we report on the physical setting and microbiology of interdune sabkhas among the large dunes in the Rub'' al Khali (the Empty Quarter) in Liwa Oasis, United Arab Emirates. The salt flats, composed of gypsum and halite, are moistened by relatively fresh ground water. The result is a salinity gradient that is inverted compared to most salt flat communities with the hypersaline layer at the top and freshwater layers below. We describe and characterize a rich photosynthetically-based microbial ecosystem that is protected from the arid outside environment by a translucent salt crust. Gases collected from sediments under shallow ponds in the sabkha contain methane in concentrations as high as 3400 ppm. The salt crust could preserve biomarkers and other evidence for life in the salt after it dries out. Chloride-filled depressions have been identified on Mars and although surface flow of water is unlikely on Mars today, ground water is possible. Such a near surface system with modern groundwater flowing under ancient salt deposits could be present on Mars and could be accessed by surface rovers.     

地球熔岩管道微生物研究对天体生物学的启示

天体生物学作为与深空探测相结合的交叉学科,旨在从地球极端环境类比、古代生命载体信息发掘和模拟等方面揭示地外行星体是否适合生命生存和繁衍,其中适宜的环境条件是评价所有天体是否宜居的重要条件。近年来在月球和火星等行星表面发现了大量由火山熔岩流形成的熔岩管道,这些巨型管状地下空间具有稳定的温度和防辐射等环境条件,为生物在地外星体上的生存提供了潜在的庇护场所。基于地球熔岩管道的天体生物学的类比研究可以为探索地外生命痕迹提供重要线索,本文综述了现阶段地球熔岩管道内微生物的研究进展、微生物痕量气体代谢在天体生物学研究中的潜力及天体生物学的研究进展,旨在为后续开展地球及地外熔岩管道的天体生物学研究提供思路。     

Metagenomics of microbial and viral life in terrestrial geothermal environments

Geothermally heated regions of Earth, such as terrestrial volcanic areas (fumaroles, hot springs, and geysers) and deep-sea hydrothermal vents, represent a variety of different environments populated by extremophilic archaeal and bacterial microorganisms. Since most of these microbes thriving in such harsh biotopes, they are often recalcitrant to cultivation; therefore, ecological, physiological and phylogenetic studies of these microbial populations have been hampered for a long time. More recently, culture-independent methodologies coupled with the fast development of next generation sequencing technologies as well as with the continuous advances in computational biology, have allowed the production of large amounts of metagenomic data. Specifically, these approaches have assessed the phylogenetic composition and functional potential of microbial consortia thriving within these habitats, shedding light on how extreme physico-chemical conditions and biological interactions have shaped such microbial communities. Metagenomics allowed to better understand that the exposure to an extreme range of selective pressures in such severe environments, accounts for genomic flexibility and metabolic versatility of microbial and viral communities, and makes extreme- and hyper-thermophiles suitable for bioprospecting purposes, representing an interesting source for novel thermostable proteins that can be potentially used in several industrial processes.     

Isolation of UVC-Tolerant Bacteria from the Hyperarid Atacama Desert, Chile

Martian surface microbial inhabitants would be challenged by a constant and unimpeded flux of UV radiation, and the study of analog model terrestrial environments may be of help to understand how such life forms could survive under this stressful condition. One of these environments is the Atacama Desert (Chile), a well-known Mars analog due to its extreme dryness and intense solar UV radiation. Here, we report the microbial diversity at five locations across this desert and the isolation of UVC-tolerant microbial strains found in these sites. Denaturing gradient gel electrophoresis (DGGE) of 16S rDNA sequences obtained from these sites showed banding patterns that suggest distinct and complex microbial communities. Analysis of 16S rDNA sequences obtained from UV-tolerant strains isolated from these sites revealed species related to the Bacillus and Pseudomonas genera. Vegetative cells of one of these isolates, Bacillus S3.300-2, showed the highest UV tolerance profile (LD₁₀?=?318 J?m²), tenfold higher than a wild-type strain of Escherichia coli. Thus, our results show that the Atacama Desert harbors a noteworthy microbial community that may be considered for future astrobiological-related research in terms of UV tolerance.     

Population and community level approaches for analysing microbial diversity in natural environments

The enormous diversity available at the microbial level is just beginning to be realized. The richness of diversity amongst the bacteria that have been described so far is between 2 and 3000, whereas estimates indicates that millions of microorganisms still remains to be discovered. Microbiologists have realized that there are at least a dozen major evolutionary groups of the microbial life forms on earth (bacteria, fungi, algae and protozoa) that are even more diverse than the better known animal and plant kingdom. Indeed, we can state that microorganisms dominate the tree of life. Microorganisms have inhabited Earth for more than 3.7 billion years, whereas plants and animals have evolved rather recently in Earth's history. Possible reports of evidence for microbial life on Mars is also consistent with the concept that microorganisms precede plants and animals on Earth. The applications of molecular-phylogenetic techniques have provided the tools for studying natural microbial communities, including those that we are not able to grow in the laboratory. The utilization of these techniques has resulted in the discovery of many new evolutionary lineages, some of them only distantly related to known organisms. Here I discuss some environmental factors controlling bacterial diversity in different environments and the utility of modern methods developed for describing this diversity.     

Life at extreme elevations on Atacama volcanoes: the closest thing to Mars on Earth?

Here we describe recent breakthroughs in our understanding of microbial life in dry volcanic tephra (“soil”) that covers much of the surface area of the highest elevation volcanoes on Earth. Dry tephra above 6000 m.a.s.l. is perhaps the best Earth analog for the surface of Mars because these “soils” are acidic, extremely oligotrophic, exposed to a thin atmosphere, high UV fluxes, and extreme temperature fluctuations across the freezing point. The simple microbial communities found in these extreme sites have among the lowest alpha diversity of any known earthly ecosystem and contain bacteria and eukaryotes that are uniquely adapted to these extreme conditions. The most abundant eukaryotic organism across the highest elevation sites is a Naganishia species that is metabolically versatile, can withstand high levels of UV radiation and can grow at sub-zero temperatures, and during extreme diurnal freeze–thaw cycles (e.g. ??10 to +?30 °C). The most abundant bacterial phylotype at the highest dry sites sampled (6330 m.a.s.l. on Volcán Llullaillaco) belongs to the enigmatic B12-WMSP1 clade which is related to the Ktedonobacter/Thermosporothrix clade that includes versatile organisms with the largest known bacterial genomes. Close relatives of B12-WMSP1 are also found in fumarolic soils on Volcán Socompa and in oligotrophic, fumarolic caves on Mt. Erebus in Antarctica. In contrast to the extremely low diversity of dry tephra, fumaroles found at over 6000 m.a.s.l. on Volcán Socompa support very diverse microbial communities with alpha diversity levels rivalling those of low elevation temperate soils. Overall, the high-elevation biome of the Atacama region provides perhaps the best “natural experiment” in which to study microbial life in both its most extreme setting (dry tephra) and in one of its least extreme settings (fumarolic soils).     

The Most Conserved Genome Segments for Life Detection on Earth and Other Planets

On Earth, very simple but powerful methods to detect and classify broad taxa of life by the polymerase chain reaction (PCR) are now standard practice. Using DNA primers corresponding to the 16S ribosomal RNA gene, one can survey a sample from any environment for its microbial inhabitants. Due to massive meteoritic exchange between Earth and Mars (as well as other planets), a reasonable case can be made for life on Mars or other planets to be related to life on Earth. In this case, the supremely sensitive technologies used to study life on Earth, including in extreme environments, can be applied to the search for life on other planets. Though the 16S gene has become the standard for life detection on Earth, no genome comparisons have established that the ribosomal genes are, in fact, the most conserved DNA segments across the kingdoms of life. We present here a computational comparison of full genomes from 13 diverse organisms from the Archaea, Bacteria, and Eucarya to identify genetic sequences conserved across the widest divisions of life. Our results identify the 16S and 23S ribosomal RNA genes as well as other universally conserved nucleotide sequences in genes encoding particular classes of transfer RNAs and within the nucleotide binding domains of ABC transporters as the most conserved DNA sequence segments across phylogeny. This set of sequences defines a core set of DNA regions that have changed the least over billions of years of evolution and provides a means to identify and classify divergent life, including ancestrally related life on other planets.     

Antarctic microbial diversity: the basis of polar ecosystem processes

Microorganisms are fundamental to the functioning of Antarctic ecosystems. Although microbial biomass can be immense in Southern Ocean blooms and freshwater cyanobacterial mats, species richness is generally more restricted than it is in temperate regions. However, there are representatives of a broad variety of taxa providing a diverse gene pool. Species diversity may be low while metabolic flexibility is high so that a few strains can provide most necessary functions. In this context, biodiversity is the sum of biological potential. This Special Issue highlights aspects of microbial ecology that can be studied only in Antarctica or which are defined most clearly in Antarctic habitats. Relatively simple microbial communities, or conspicuous species within them, can be used as indicators of microbial processes and responses to environmental change. These include the palaeological record of benthic diatoms and response of soil cyanobacterial communities to regional warming and UV-B stress. The climatic conditions and relict babitats of the Antarctic dry valleys are a valuable analogue for detecting microbial life and diversity on Mars. The global microbial biodiversity initiative Diversitas and international Antarctic networks such as BIOTAS (Biological Investigations of Terrestrial Antarctic Systems) harness taxonomic and ecophysiological expertize to understand better these unique polar ecosystems.     

Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction

Iron (Fe) has long been a recognized physiological requirement for life, yet for many microorganisms that persist in water, soils and sediments, its role extends well beyond that of a nutritional necessity. Fe(II) can function as an electron source for iron-oxidizing microorganisms under both oxic and anoxic conditions and Fe(III) can function as a terminal electron acceptor under anoxic conditions for iron-reducing microorganisms. Given that iron is the fourth most abundant element in the Earth's crust, iron redox reactions have the potential to support substantial microbial populations in soil and sedimentary environments. As such, biological iron apportionment has been described as one of the most ancient forms of microbial metabolism on Earth, and as a conceivable extraterrestrial metabolism on other iron-mineral-rich planets such as Mars. Furthermore, the metabolic versatility of the microorganisms involved in these reactions has resulted in the development of biotechnological applications to remediate contaminated environments and harvest energy.     

Life at the dry edge: Microorganisms of the Atacama Desert

The Atacama Desert, located in northern Chile, is the driest and oldest Desert on Earth. Research aimed at the understanding of this unique habitat and its diverse microbial ecosystems begun only a few decades ago, mainly driven by NASA's astrobiology program. A milestone in these efforts was a paper published in 2003, when the Atacama was shown to be a proper model of Mars. From then on, studies have been focused to examine every possible niche suitable for microbial life in this extreme environment. Habitats as different as the underside of quartz rocks, fumaroles at the Andes Mountains, the inside of halite evaporates and caves of the Coastal Range, among others, have shown that life has found ingenious ways to adapt to extreme conditions such as low water availability, high salt concentration and intense UV radiation.     

Feast and famine--microbial life in the deep-sea bed

The seabed is a diverse environment that ranges from the desert-like deep seafloor to the rich oases that are present at seeps, vents, and food falls such as whales, wood or kelp. As well as the sedimentation of organic material from above, geological processes transport chemical energy--hydrogen, methane, hydrogen sulphide and iron--to the seafloor from the subsurface below, which provides a significant proportion of the deep-sea energy. At the sites on the seafloor where chemical energy is delivered, rich and diverse microbial communities thrive. However, most subsurface microorganisms live in conditions of extreme energy limitation, with mean generation times of up to thousands of years. Even in the most remote subsurface habitats, temperature rather than energy seems to set the ultimate limit for life, and in the deep biosphere, where energy is most depleted, life might even be based on the cleavage of water by natural radioisotopes. Here, we review microbial biodiversity and function in these intriguing environments.     

Current state of athalassohaline deep-sea hypersaline anoxic basin research—recommendations for future work and relevance to astrobiology

Deep-sea hypersaline anoxic basins (DHABs) are uniquely stratified polyextreme environments generally found in enclosed seas. These environments select for elusive and widely uncharacterized microbes that may be living below the currently recognized window of life on Earth. Still, there is strong evidence of highly specialized active microbial communities in the Kryos, Discovery, and Hephaestus basins located in the Eastern Mediterranean Sea; the only known athalassohaline DHABs. Life is further constrained in these DHABs as near-saturated concentrations of magnesium chloride significantly reduces water activity (a_w) and exerts extreme chaotropic stress, the tendency of a solution to disorder biomolecules. In this review, we provide an overview of microbial adaptations to polyextremes focusing primarily on chaotropicity, summarize current evidence of microbial life within athalassohaline DHABs and describe the difficulties of life detection approaches and sampling within these environments. We also reveal inconsistent measurements of chaotropic activity in the literature highlighting the need for a new methodology. Finally, we generate recommendations for future investigations and discuss the importance of athalassohaline DHAB research to help inform extraterrestrial life detection missions.     

Elucidating the ecological networks in stone-dwelling microbiomes

Stone surfaces are extreme environments that support microbial life. This microbial growth occurs despite unfavourable conditions associated with stone including limited sources of nutrients and water, high pH and exposure to extreme variations in temperature, humidity and irradiation. These stone-dwelling microbes are often resistant to extreme environments including exposure to desiccation, heavy metals, UV and Gamma irradiation. Here, we report on the effects of climate and stone geochemistry on microbiomes of Roman stone ruins in North Africa. Stone microbiomes were dominated by Actinobacteria, Cyanobacteria and Proteobacteria but were heavily impacted by climate variables that influenced water availability. Stone geochemistry also influenced community diversity, particularly through biologically available P, Mn and Zn. Functions associated with photosynthesis and UV protection were enriched in the metagenomes, indicating the significance of these functions for community survival on stones. Core members of the stone microbial communities were also identified and included Geodermatophilaceae, Rubrobacter, Sphingomonas and others. Our research has helped to expand the understanding of stone microbial community structure and functional capacity within the context of varying climates, geochemical properties and stone conditions.     

Extremotolerance in fungi: evolution on the edge

Our planet offers many opportunities for life on the edge: high and low temperatures, high salt concentrations, acidic and basic conditions and toxic environments, to name but a few extremes. Recent studies have revealed the diversity of fungi that can occur in stressful environments that are hostile to most eukaryotes. We review these studies here, with the additional purpose of proposing some mechanisms that would allow for the evolutionary adaptation of eukaryotic microbial life under extreme conditions. We focus, in particular, on life in ice and life at high salt concentrations, as there is a surprising similarity between the fungal populations in these two kinds of environments, both of which are characterized by low water activity. We propose steps of evolution of generalist species towards the development of specialists in extreme habitats. We argue that traits present in some fungal groups, such as asexuality, synthesis of melanin-like pigments and a flexible morphology, are preadaptations that facilitate persistence and eventual adaptation to conditions on the ecological edge, as well as biotope switches. These processes are important for understanding the evolution of extremophiles; moreover, they have implications for the emergence of novel fungal pathogens.     

Life: past, present and future

Molecular methods of taxonomy and phylogeny have changed the way in which life on earth is viewed; they have allowed us to transition from a eukaryote-centric (five-kingdoms) view of the planet to one that is peculiarly prokarote-centric, containing three kingdoms, two of which are prokaryotic unicells. These prokaryotes are distinguished from their eukaryotic counterparts by their toughness, tenacity and metabolic diversity. Realization of these features has, in many ways, changed the way we feel about life on earth, about the nature of life past and about the possibility of finding life elsewhere. In essence, the limits of life on this planet have expanded to such a degree that our thoughts of both past and future life have been altered. The abilities of prokaryotes to withstand many extreme conditions has led to the term extremophiles, used to describe the organisms that thrive under conditions thought just a few years ago, to be inconsistent with life. Perhaps the most extensive adaptation to extreme conditions, however, is represented by the ability of many bacteria to survive nutrient conditions not compatible with eukaryotic life. Prokaryotes have evolved to use nearly every redox couple that is in abundance on earth, filling the metabolic niches left behind by the oxygen-using, carbon-eating eukaryotes. This metabolic plasticity leads to a common feature in physically stratified environments of layered microbial communities, chemical indicators of the metabolic diversity of the prokaryotes. Such 'metabolic extremophily' forms a backdrop by which we can view the energy flow of life on this planet, think about what the evolutionary past of the planet might have been, and plan ways to look for life elsewhere, using the knowledge of energy flow on earth.     

High-throughput molecular analyses of microbiomes as a tool to monitor the wellbeing of aquatic environments

Aquatic environments are the recipients of many sources of environmental stress that trigger both local and global changes. To evaluate the associated risks to organisms and ecosystems more sensitive and accurate strategies are required. The analysis of the microbiome is one of the most promising candidates for environmental diagnosis of aquatic systems. Culture-independent interconnected meta-omic approaches are being increasing used to fill the gaps that classical microbial approaches cannot resolve. Here, we provide a prospective view of the increasing application of these high-throughput molecular technologies to evaluate the structure and functional activity of microbial communities in response to changes and disturbances in the environment, mostly of anthropogenic origin. Some relevant topics are reviewed, such as: (i) the use of microorganisms for water quality assessment, highlighting the incidence of antimicrobial resistance as an increasingly serious threat to global public health; (ii) the crucial role of microorganisms and their complex relationships with the ongoing climate change, and other stress threats; (iii) the responses of the environmental microbiome to extreme pollution conditions, such as acid mine drainage or oil spills. Moreover, protists and viruses, due to their huge impacts on the structure of microbial communities, are emerging candidates for the assessment of aquatic environmental health.     

Probabilistic Models to Describe the Dynamics of Migrating Microbial Communities

In all but the most sterile environments bacteria will reside in fluid being transported through conduits and some of these will attach and grow as biofilms on the conduit walls. The concentration and diversity of bacteria in the fluid at the point of delivery will be a mix of those when it entered the conduit and those that have become entrained into the flow due to seeding from biofilms. Examples include fluids through conduits such as drinking water pipe networks, endotracheal tubes, catheters and ventilation systems. Here we present two probabilistic models to describe changes in the composition of bulk fluid microbial communities as they are transported through a conduit whilst exposed to biofilm communities. The first (discrete) model simulates absolute numbers of individual cells, whereas the other (continuous) model simulates the relative abundance of taxa in the bulk fluid. The discrete model is founded on a birth-death process whereby the community changes one individual at a time and the numbers of cells in the system can vary. The continuous model is a stochastic differential equation derived from the discrete model and can also accommodate changes in the carrying capacity of the bulk fluid. These models provide a novel Lagrangian framework to investigate and predict the dynamics of migrating microbial communities. In this paper we compare the two models, discuss their merits, possible applications and present simulation results in the context of drinking water distribution systems. Our results provide novel insight into the effects of stochastic dynamics on the composition of non-stationary microbial communities that are exposed to biofilms and provides a new avenue for modelling microbial dynamics in systems where fluids are being transported.