Biomineralization of endolithic microbes in rocks from the McMurdo Dry Valleys of Antarctica: implications for microbial fossil formation and their detection

In some zones of Antarctica's cold and dry desert, the extinction of cryptoendolithic microorganisms leaves behind inorganic traces of microbial life. In this paper, we examine the transition from live microorganisms, through their decay, to microbial fossils using in situ microscopy (transmission electron microscopy, scanning electron microscopy in back-scattered electron mode) and microanalytical (energy dispersive X-ray spectroscopy) techniques. Our results demonstrate that, after their death, endolithic microorganisms inhabiting Commonwealth Glacier sandstone from the Antarctica McMurdo Dry Valleys become mineralized. In some cases, epicellular deposition of minerals and/or simply filling up of empty moulds by minerals leads to the formation of cell-shaped structures that may be considered biomarkers. The continuous deposition of allochthonous clay minerals and sulfate-rich salts fills the sandstone pores. This process can give rise to microbial fossils with distinguishable cell wall structures. Often, fossilized cell interiors were of a different chemical composition to the mineralized cell walls. We propose that the microbial fossil formation observed was induced by mineral precipitation resulting from inorganic processes occurring after the death of cryptoendolithic microorganisms. Nevertheless, it must have been the organic template that provoked the diffusion of mineral elements and gave rise to their characteristic distribution pattern inside the fossilized cells.     

Iron-Rich Diagenetic Minerals are Biomarkers of Microbial Activity in Antarctic Rocks

The cold, dry ecosystems of Antarctica have been shown to harbor traces left behind by microbial activity within certain types of rocks, but only two indirect biomarkers of cryptoendolithic activity in the Antarctic cold desert zone have been described to date. These are the geophysical and geochemical bioweathering patterns macroscopically observed in sandstone rock. Here we show that in this extreme environment, minerals are biologically transformed, and as a result, Fe-rich diagenetic minerals in the form of iron hydroxide nanocrystals and biogenic clays are deposited around chasmoendolithic hyphae and bacterial cells. Thus, when microbial life decays, these characteristic neocrystalized minerals act as distinct biomarkers of previous endolithic activity. The ability to recognize these traces may have potential astrobiological implications because the Antarctic Ross Desert is considered a terrestrial analogue of a possible ecosystem on early Mars.     

Extreme environments and exobiology

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.     

Life, decay and fossilisation of endolithic microorganisms from the Ross Desert, Antarctica

The adaptation and survival of the endolithic microorganisms that colonise the near-surface layer of porous sandstone rock in the Ross Desert (Antarctica) depend upon a precarious equilibrium of biological, geological and climatic factors. Any unfavourable change in external conditions can result in the death and disappearance of microscopic organisms, and this may be followed by trace microfossil formation. The sequence of events leading to the extinction of life in the Antarctic desert is considered to be a terrestrial analogue of the disappearance of possible life on early Mars. The present paper reviews the current state of knowledge on the endolithic microorganisms of the Ross Desert with particular reference to their decay and fossilisation processes. Ideas for in situ further research on this microbial ecosystem are also proposed, including several new microscopy techniques such as CLSM, LTSEM, SEM-BSE and EDS. Preliminary images are presented and it is proposed that, for the first time, such techniques will permit the in situ study of the ecology of Antarctic lithobiontic microorganisms and the identification and characterisation of fossilised traces of past life.     

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.     

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.     

Microbial life in glacial ice and implications for a cold origin of life

Application of physical and chemical concepts, complemented by studies of prokaryotes in ice cores and permafrost, has led to the present understanding of how microorganisms can metabolize at subfreezing temperatures on Earth and possibly on Mars and other cold planetary bodies. The habitats for life at subfreezing temperatures benefit from two unusual properties of ice. First, almost all ionic impurities are insoluble in the crystal structure of ice, which leads to a network of micron-diameter veins in which microorganisms may utilize ions for metabolism. Second, ice in contact with mineral surfaces develops a nanometre-thick film of unfrozen water that provides a second habitat that may allow microorganisms to extract energy from redox reactions with ions in the water film or ions in the mineral structure. On the early Earth and on icy planets, prebiotic molecules in veins in ice may have polymerized to RNA and polypeptides by virtue of the low water activity and high rate of encounter with each other in nearly one-dimensional trajectories in the veins. Prebiotic molecules may also have utilized grain surfaces to increase the rate of encounter and to exploit other physicochemical features of the surfaces.     

矿物电子能量协同微生物胞外电子传递与生长代谢

矿物是无机自然界吸收与转化能量的重要载体,其与微生物的胞外电子传递过程体现出矿物电子能量对微生物生长代谢与能量获取方式的影响。根据电子来源与产生途径,以往研究表明矿物中变价元素原子最外层或次外层价电子与半导体矿物导带上的光电子是微生物可以利用的两种不同胞外电子能量形式,其产生及传递方式与微生物胞外电子传递的电子载体密切相关。在协同微生物胞外电子传递过程中,矿物不同电子能量形式之间既有相似性亦存在着差异。反过来,微生物胞内-胞外电子传递途径也影响对矿物电子能量的吸收与获取,进而对微生物生长代谢等生命活动产生影响。本文在阐述矿物不同电子能量形式产生机制及其参与生物化学反应的共性和差异性特征基础上,综述了微生物获取矿物电子能量所需的不同电子载体类型与传递途径,探讨了矿物不同电子能量形式对微生物生长代谢等生命活动的影响,展望了自然条件下微生物利用矿物电子能量调节其生命活动、调控元素与能量循环的新方式。     

稳定性同位素探测技术在微生物生态学研究中的应用

稳定性同位素标记技术同分子生物学技术相结合而发展起来的稳定性同位素探测技术（stableisotope probing,SIP）,在对各种环境中微生物群落组成进行遗传分类学鉴定的同时,可确定其在环境过程中的功能,提供复杂群落中微生物相互作用及其代谢功能的大量信息,具有广阔的应用前景.其基本原理是：将原位或微宇宙（microcosm）的环境样品暴露于稳定性同位素富集的基质中,这些样品中存在的某些微生物能够以基质中的稳定（性同位素为碳源或氮源进行物质代谢并满足其自身生长需要,基质中的稳定性同位素被吸收同化进入微生物体内,参与各类物质如核酸（DNA和RNA）及磷脂脂肪酸（PLFA）等的生物合成,通过提取、分离、纯化、分析这些微生物体内稳定性同位素标记的生物标志物,从而将微生物的组成与其功能联系起来.在介绍稳定性同位素培养基质的选择及标记方法、合适的生物标志物的选择及提取分离方法的基础上,举例阐述了此项技术在甲基营养菌、有机污染物降解菌、根际微生物生态、互营微生物、宏基因组学等方面的应用.     

Experimental silicification of the extremophilic Archaea Pyrococcus abyssi and Methanocaldococcus jannaschii: applications in the search for evidence of life in early Earth and extraterrestrial rocks

Hydrothermal activity was common on the early Earth and associated micro‐organisms would most likely have included thermophilic to hyperthermophilic species. 3.5–3.3 billion‐year‐old, hydrothermally influenced rocks contain silicified microbial mats and colonies that must have been bathed in warm to hot hydrothermal emanations. Could they represent thermophilic or hyperthermophilic micro‐organisms and if so, how were they preserved? We present the results of an experiment to silicify anaerobic, hyperthermophilic micro‐organisms from the Archaea Domain Pyrococcus abyssi and Methanocaldococcus jannaschii, that could have lived on the early Earth. The micro‐organisms were placed in a silica‐saturated medium for periods up to 1 year. Pyrococcus abyssi cells were fossilized but the M. jannaschii cells lysed naturally after the exponential growth phase, apart from a few cells and cell remains, and were not silicified although their extracellular polymeric substances were. In this first simulated fossilization of archaeal strains, our results suggest that differences between species have a strong influence on the potential for different micro‐organisms to be preserved by fossilization and that those found in the fossil record represent probably only a part of the original diversity. Our results have important consequences for biosignatures in hydrothermal or hydrothermally influenced deposits on Earth, as well as on early Mars, as environmental conditions were similar on the young terrestrial planets and traces of early Martian life may have been similarly preserved as silicified microfossils.     

Colonization of nascent, deep-sea hydrothermal vents by a novel Archaeal and Nanoarchaeal assemblage

Active deep-sea hydrothermal vents are areas of intense mixing and severe thermal and chemical gradients, fostering a biotope rich in novel hyperthermophilic microorganisms and metabolic pathways. The goal of this study was to identify the earliest archaeal colonizers of nascent hydrothermal chimneys, organisms that may be previously uncharacterized as they are quickly replaced by a more stable climax community. During expeditions in 2001 and 2002 to the hydrothermal vents of the East Pacific Rise (EPR) (9 degrees 50'N, 104 degrees 17'W), we removed actively venting chimneys and in their place deployed mineral chambers and sampling units that promoted the growth of new, natural hydrothermal chimneys and allowed their collection within hours of formation. These samples were compared with those collected from established hydrothermal chimneys from EPR and Guaymas Basin vent sites. Using molecular and phylogenetic analysis of the 16S rDNA, we show here that at high temperatures, early colonization of a natural chimney is dominated by members of the archaeal genus Ignicoccus and its symbiont, Nanoarchaeum. We have identified 19 unique sequences closely related to the nanoarchaeal group, and five archaeal sequences that group closely with Ignicoccus. These organisms were found to colonize a natural, high temperature protochimney and vent-like mineral assemblages deployed over high temperature outflows within 92 h. When compared phylogenetically, several of these colonizing organisms form a unique clade independent of those found in mature chimneys and low-temperature mineral chamber samples. As a model ecosystem, the identification of pioneering consortia in deep-sea hydrothermal vents may help advance the understanding of how early microbial life forms gained a foothold in hydrothermal systems on early Earth and potentially on other planetary bodies.     

Effect of hydrogen peroxide and hydrated ferric oxides on the metabolism of soil microflora

The effect of hydrogen peroxide and the mineral limonite on the rate of microbial processes was studied in poor and rich soils. The dynamics of CO2 evolution can be registered upon addition of hydrogen peroxide to chernozem samples, which confirms the existence of metabolism of soil microorganisms. In experiments with desert soil, the evolution of O2 increases rather than that of CO2, which is probably due to an increase in the number of microorganisms producing catalase. Limonite stimulates the metabolic activity of microrganisms. The cultural and morphological properties of microflora are described, which are typical of soils incubated in the presence of limonite and hydrogen peroxide. This work supports the conclusion that, theoretically, the ground of Mars may contain microorganisms which have adapted, in the course of evolution, to high concentrations of hydrogen peroxide and hydrated iron oxides (of the limonite type) in the surrounding medium.     

Way to the detection of Mars life]

In this review, I would like to introduce how we can detect the possible life on Mars. Even though the quantitative estimation of the possibility of biogenesis on Mars is difficult, Dr. McKay and his colleagues work has thrown a tiny light for this possibility. Considering Mars environmental conditions, the possible life is microorganisms. The detection of microorganisms in natural environments is not easy even on Earth due to the premature detection technique. We have developed a method based on the fluorescence microscopic technique. This method proved to be successful for the detection of terrestrial microorganisms. Even some pre-biotic cells can be detected. We are developing a miniature detection apparatus which meet the required standard for installing on the Mars landers. We also propose the ground based experiments using Martian meteorites or pseudo-Martian rocks.     

Search for bioorganic compounds and organisms on Mars

A prototype of new instrument is under construction as a part of Russian Mars program to search for bioorganic compounds and microorganisms which might be frozen in rock under the places where the traces of water were found or near the poles of Mars. The proposed instrument consists of a quadrupole mass spectrometer (QMS) to detect chemical compounds and a fluorescent microscope system (FMS) to detect organisms and bioorganic compounds in bulk.     

Engineering issues of microbial ecology in space agriculture]

Closure of the materials recycle loop for water-foods-oxygen is the primary purpose of space agriculture on Mars and Moon. A microbial ecological system takes a part of agriculture to process our metabolic excreta and inedible biomass and convert them to nutrients and soil substrate for cultivating plants. If we extend the purpose of space agriculture to the creation and control of a healthy and pleasant living environment, we should realize that our human body should not be sterilized but exposed to the appropriate microbial environment. We are proposing a use of hyper-thermophilic aerobic composting microbial ecology in space agriculture. Japan has a broad historical and cultural background on this subject. There had been agriculture that drove a closed loop of materials between consuming cities and farming villages in vicinity. Recent environmental problems regarding garbage collection and processing in towns have motivated home electronics companies to innovate "garbage composting" machines with bacterial technology. Based on those matured technology, together with new insights on microbiology and microbial ecology, we have been developing a conceptual design of space agriculture on Moon and Mars. There are several issues to be answered in order to prove effectiveness of the use of microbial systems in space. 1) Can the recycled nutrients, processed by the hyper-thermal aerobic composting microbial ecology, be formed in the physical and chemical state or configuration, with which plants can uptake those nutrients? A possibility of removing any major components of fertilizer from its recycle loop is another item to be evaluated. 2) What are the merits of forming soil microbial ecology around the root system of plants? This might be the most crucial question. Recent researches exhibit various mutually beneficial relationships among soil microbiota and plants, and symbiotic ecology in composting bacteria. It is essential to understand those features, and define how to conduct preventive maintenance for keeping cultivating soil healthy and productive. 3) Does microbial ecology contribute to building sustainable and expandable human habitation by utilizing the on site extraterrestrial resources? We are assessing technical feasibility of converting regolith to farming soil and structural materials for space agriculture. In the case of Mars habitation, carbon dioxide and a trace amount of nitrogen in atmosphere, and potassium and phosphor in minerals are the sources we consider. Excess oxygen can be accumulated by woods cultivation and their use for lumber. 4) Is the operation of space agriculture robust and safe, if it adopts hyper-thermophilic aerobic microbial ecology? Any ecological system is complex and non-linear, and shows latency and memory effects in its response. It is highly important to understand those features to design and operate space agriculture without falling into the fatal failure. Assessment should be made on the microbial safety and preparation of the preventive measures to eliminate negative elements that would either retard agricultural production or harm the healthy environment. It is worth to mention that such space agriculture would be an effective engineering testbed to solve the global problem on energy and environment. Mars and Moon exploration itself is a good advocate of healthy curiosity expressed by the sustainable civilization of our humankind. We propose to work together towards Mars and Moon with microbial ecology to assure pleasant habitation there.     

Deconstructing Earth’s oldest ichnofossil record from the Pilbara Craton,West Australia: Implications for seeking life in the Archean subseafloor

Microtextures of titanite (CaTiSiO₅) in exceptionally preserved Archean pillow lavas have been proposed as the earliest examples of microbial ichnofossils. An origin from microbial tunneling of seafloor volcanic glass that is subsequently chloritized and the tunnels infilled by titanite has been argued to record the activities of subseafloor microbes. We investigate the evidence in pillow lavas of the 3.35 Ga Euro Basalt from the Pilbara Craton, Western Australia, to evaluate the biogenicity of the microtextures. We employ a combination of light microscopy and chlorite mineral chemical analysis by EPMA (electron probe micro‐analysis) to document the environment of formation and analyze their ultrastructure using FIB‐TEM (focussed ion beam combined with transmission electron microscopy) to investigate their mode of growth. Petrographic study of the original and re‐collected material identified an expanded range of titanite morphotypes along with early anatase growth forming chains and aggregates of coalesced crystallites in a sub‐greenschist facies assemblage. High‐sensitivity mapping of FIB lamellae cut across the microtextures confirm that they are discontinuous chains of coalesced crystallites that are highly variable in cross section and contain abundant chlorite inclusions, excluding an origin from the mineralization of previously hollow microtunnels. Comparison of chlorite mineral compositions to DSDP/IODP data reveals that the Euro Basalt chlorites are similar to recent seafloor chlorites. We advance an abiotic origin for the Euro Basalt microtextures formed by spontaneous nucleation and growth of titanite and/anatase during seafloor‐hydrothermal metamorphism. Our findings reveal that the Euro Basalt microtextures are not comparable to microbial ichnofossils from the recent oceanic crust, and we question the evidence for life in these Archean lavas. The metamorphic reactions that give rise to the growth of the Euro Basalt microtextures could be commonplace in Archean pillow lavas and need to be excluded when seeking traces of life in the subseafloor on the early Earth.     

城市绿地微生物及其对城市化的响应

城市绿地微生物的稳定性是城市绿地发挥其重要生态系统功能的重要因素。人类世时代的快速城市化会改变城市绿地土壤理化性质、输入新兴污染物、加剧微生物生态系统潜在风险、改变微生物群落多样性及生态系统功能多样性,深远地影响了城市绿地的生态系统服务功能。本文综述了城市绿地微生物的特征,以及城市化进程对城市绿地微生物组(包括土壤、植物叶际和空气)、抗生素抗性基因、病原微生物和稀有物种群落的影响。与自然微生物相比,城市绿地微生物普遍具有较高的异质性,受人类活动影响大。同时,抗生素抗性基因水平以及人类致病菌数量则显著增加,体现了城市化对城市绿地生态系统健康和功能的扰动。今后研究中应更加关注城市化对于城市绿地微生物的影响,为其对人群健康影响风险评价提供可靠理论支持。     

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。     

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.