The diversity and abundance of bacteria inhabiting seafloor lavas positively correlate with rock alteration

Young, basaltic ocean crust exposed near mid-ocean ridge spreading centers present a spatially extensive environment that may be exploited by epi- and endolithic microbes in the deep sea. Geochemical energy released during basalt alteration reactions can theoretically support chemosynthesis, contributing to a trophic base for the ocean crust biome. To examine associations between endolithic microorganisms and basalt alteration processes, we compare the phylogenetic diversity, abundance and community structure of bacteria existing in several young, seafloor lavas from the East Pacific Rise at ∼9°N that are variably affected by oxidative seawater alteration. The results of 16S rRNA gene analyses and real-time, quantitative polymerase chain reaction measurements show that the abundance of prokaryotic communities, dominated by the bacterial domain, positively correlates with the extent of rock alteration – the oldest, most altered basalt harbours the greatest microbial biomass. The bacterial community overlap, structure and species richness relative to alteration state is less explicit, but broadly corresponds to sample characteristics (type of alteration products and general alteration state). Phylogenetic analyses suggest that the basalt biome may contribute to the geochemical cycling of Fe, S, Mn, C and N in the deep sea.     

Diversity of endolithic fungal communities in dolomite and limestone rocks from Nanjiang Canyon in Guizhou karst area, China

The endolithic environment, the tiny pores and cracks in rocks, buffer microbial communities from a number of physical stresses, such as desiccation, rapid temperature variations, and UV radiation. Considerable knowledge has been acquired about the diversity of microorganisms in these ecosystems, but few culture-independent studies have been carried out on the diversity of fungi to date. Scanning electron microscopy of carbonate rock fragments has revealed that the rock samples contain certain kinds of filamentous fungi. We evaluated endolithic fungal communities from bare dolomite and limestone rocks collected from Nanjiang Canyon (a typical karst canyon in China) using culture-independent methods. Results showed that Ascomycota was absolutely dominant both in the dolomite and limestone fungal clone libraries. Basidiomycota and other eukaryotic groups (Bryophyta and Chlorophyta) were only detected occasionally or at low frequencies. The most common genus in the investigated carbonate rocks was Verrucaria. Some other lichen-forming fungi (e.g., Caloplaca, Exophiala, and Botryolepraria), Aspergillus, and Penicillium were also identified from the rock samples. The results provide a cross-section of the endolithic fungal communities in carbonate rocks and help us understand more about the role of microbes (fungi and other rock-inhabiting microorganisms) in rock weathering and pedogenesis.     

Geomicrobiology in oceanography: microbe-mineral interactions at and below the seafloor

Oceanography is inherently interdisciplinary and, since its inception, has included the study of microbe-mineral interactions. From early studies of manganese nodules, to the discovery of hydrothermal vents, it has been recognized that microorganisms are involved at various levels in the transformation of rocks and minerals at and below the seafloor. Recent studies include mineral weathering at low temperatures and microbe-mineral interactions in the subseafloor "deep biosphere". A common characteristic of seafloor and subseafloor geomicrobiological processes that distinguishes them from terrestrial or near-surface processes is that they occur in the dark, one or more steps removed from the sunlight that fuels the near-surface biosphere on Earth. This review focuses on geomicrobiological studies and energy flow in dark, deep-ocean and subseafloor rock habitats.     

Neutrophilic Iron-Oxidizing Bacteria in the Ocean: Their Habitats,Diversity, and Roles in Mineral Deposition,Rock Alteration,and Biomass Production in the Deep-Sea

The importance of metals to life has long been appreciated. Iron (Fe) is the fourth most abundant element overall, and the second most abundant element that is redox-active in near-surface aqueous habitats, rendering it the most important environmental metal. While it has long been recognized that microorganisms participate in the global iron cycle, appreciation for the pivotal role that redox cycling of iron plays in energy conservation among diverse prokaryotes has grown substantially in the past decade. In addition, redox reactions involving Fe are linked to several other biogeochemical cycles (e.g., carbon), with significant ecological ramifications. The increasing appreciation for the role of microbes in redox transformations of Fe is reflected in a recent surge in biological and environmental studies of microorganisms that conserve energy for growth from redox cycling of Fe compounds, particularly in the deep ocean. Here we highlight some of the key habitats where microbial Fe-oxidation plays significant ecological and biogeochemical roles in the oceanic regime, and provide a synthesis of recent studies concerning this important physiological group. We also provide the first evidence that microbial Fe-oxidizing bacteria are a critical factor in the kinetics of mineral dissolution at the seafloor, by accelerating dissolution by 6–8 times over abiotic rates. We assert that these recent studies, which indicate that microbial Fe-oxidation is widespread in the deep-sea, combined with the apparent role that this group play in promoting rock and mineral weathering, indicate that a great deal more attention to these microorganisms is warranted in order to elucidate the full physiological and phylogenetic diversity and activity of the neutrophilic Fe-oxidizing bacteria in the oceans.     

Phylogenetic Composition of Rocky Mountain Endolithic Microbial Ecosystems

The endolithic environment, the pore space in rocks, is a ubiquitous microbial habitat. Photosynthesis-based endolithic communities inhabit the outer few millimeters to centimeters of rocks exposed to the surface. Such endolithic ecosystems have been proposed as simple, tractable models for understanding basic principles in microbial ecology. In order to test previously conceived hypotheses about endolithic ecosystems, we studied selected endolithic communities in the Rocky Mountain region of the United States with culture-independent molecular methods. Community compositions were determined by determining rRNA gene sequence contents, and communities were compared using statistical phylogenetic methods. The results indicate that endolithic ecosystems are seeded from a select, global metacommunity and form true ecological communities that are among the simplest microbial ecosystems known. Statistical analysis showed that biogeographical characteristics that control community composition, such as rock type, are more complex than predicted. Collectively, results of this study support the idea that patterns of microbial diversity found in endolithic communities are governed by principles similar to those observed in macroecological systems.     

Epilithic and Endolithic Bacterial Communities in Limestone from a Maya Archaeological Site

Biodeterioration of archaeological sites and historic buildings is a major concern for conservators, archaeologists, and scientists involved in preservation of the world's cultural heritage. The Maya archaeological sites in southern Mexico, some of the most important cultural artifacts in the Western Hemisphere, are constructed of limestone. High temperature and humidity have resulted in substantial microbial growth on stone surfaces at many of the sites. Despite the porous natureof limestone and the common occurrence of endolithic microorganisms in many habitats, little is known about the microbial flora living inside the stone. We found a large endolithic bacterial community in limestone from the interior of the Maya archaeological site Ek' Balam. Analysis of 16S rDNA clones demonstrated disparate communities (endolithic: >80% Actinobacteria, Acidobacteria, and Low GC Firmicutes; epilithic: >50% Proteobacteria). The presence of differing epilithic and endolithic bacterial communities may be a significant factor for conservation of stone cultural heritage materials and quantitative prediction of carbonate weathering.     

Nitrogen economy of endolithic microbial communities in hot and cold deserts

The source of combined nitrogen in endolithic microbial communities was studied in samples from desert localities in North and South America, the Middle East, South Africa, and Antarctica. Nitrogen fixation (acetylene reduction) seems to occur only exceptionally. Evidence suggests that, in general, the nitrogen source for endolithic microorganisms in deserts is abiotically fixed nitrogen produced by atmospheric electric discharges (lightning or aurorae), conveyed to the rock by atmospheric precipitation. Nitrogen is apparently not a limiting factor in these low-productivity communities. An incomplete nitrogen cycle seems to be present which includes the following pathways: supply of nitrates and ammonia from the atmosphere; decomposition of organic matter to ammonia; reassimilation of ammonia; ammonia volatilization; loss of organic matter through weathering (only in certain Antarctic rocks); biological nitrogen fixation (exceptional).     

Phylogenetic composition of Rocky Mountain endolithic microbial ecosystems

The endolithic environment, the pore space in rocks, is a ubiquitous microbial habitat. Photosynthesis-based endolithic communities inhabit the outer few millimeters to centimeters of rocks exposed to the surface. Such endolithic ecosystems have been proposed as simple, tractable models for understanding basic principles in microbial ecology. In order to test previously conceived hypotheses about endolithic ecosystems, we studied selected endolithic communities in the Rocky Mountain region of the United States with culture-independent molecular methods. Community compositions were determined by determining rRNA gene sequence contents, and communities were compared using statistical phylogenetic methods. The results indicate that endolithic ecosystems are seeded from a select, global metacommunity and form true ecological communities that are among the simplest microbial ecosystems known. Statistical analysis showed that biogeographical characteristics that control community composition, such as rock type, are more complex than predicted. Collectively, results of this study support the idea that patterns of microbial diversity found in endolithic communities are governed by principles similar to those observed in macroecological systems.     

Phylogenetic diversity of endolithic bacteria in Bole granite rock in Xinjiang

The endolithic environment is a ubiquitous microbial habitat for microorganisms, such as lichens, Cyanobacteria and fungi, and it provides mineral nutrients and growth surfaces. In extremely environments, such as hot and cold desert, endolithic communities are often the main form of life. More recently, endolithic microbial communities have been observed inhabiting a variety of rock types ranging from hard granite to porous rocks such as basalt, dolomite, limestone, sandstone and granites. Regardless of geographic location and rock type, each of these habitats is characterized by a subsurface microclimate that prevents endolithic microorganisms growth. Photosynthesis-based endolithic microbial communities commonly inhabit the outer millimeters to centimeters of rocks exposed to the surface. The ability to fix carbon dioxide and in some cases atmospheric dinitrogen, gives the Cyanobacteria a clear competitive advantage over heterotrophic bacteria, so it is been called the main primary producer. Light quality and intensity appear to be the main determinant of the maximum depth to which growth occurs in endolithic phototrophic communities. Valleys of Fantastic Rocks in Bole is close to Alashankou Port of Xinjiang which belongs to extreme continental climate. In order to investigate the structure, composition and diversity of endolithic bacterial community in exposed granitic porphyry in the Valleys of Fantastic Rocks, environmental DNA was directly extracted from granite rock, the 16S rRNA genes were amplified from the total DNA by PCR with bacterial-specific primers, and an endolithic bacterial clone library was constructed. Positive clones were randomly selected from the library and identified by Restriction Fragment Length Polymorphism (RFLP). The unique rRNA types clones were sequenced, analysised and then constructed phylogenetic tree. In total, 129 positive clones were screened and grouped into 46 operational taxonomic unites (OTUs). The clone coverage C value was 89.15%, indicating that most of the estimated endolithic bacterial diversity was sampled. BLAST analysis indicated that 46 OTUs were divided into seven phyla (Acidobacteria, Actinobacteria, Bacteroidetes, Chloroflexi, Cyanobacteria, Planctomycetes, Proteobacteria) and five unknown groups. Cyanobacteria (43%), especially the Gp I, form the functional basis for an endolithic bacteria community which contain a wide spectrum species of chemotrophic bacteria (33%) with mainly Actinobacteria, α-Proteobacteria, Acidobacteria. Additionally, most clones that derived from the endolithic bacteria clone library showed high similarity to the sequence deposited in GenBank database with 97%–99%. Besides, 35% of the clones showed less than 97% of sequence similarity, of which 12% sequences were affiliated to genus Rubrobacter. The results suggested that endolithic bacteria in Valleys of Fantastic Rocks in Xinjiang were highly diverse in species richness, and maybe have a diversity of potential novel species and lineages.     

Microscopic and biomolecular complementary approaches to characterize bioweathering processes at petroglyph sites from the Negev Desert,Israel

Throughout the Negev Desert highlands, thousands of ancient petroglyphs sites are susceptible to deterioration processes that may result in the loss of this unique rock art. Therefore, the overarching goal of the current study was to characterize the composition, diversity and effects of microbial colonization of the rocks to find ways of protecting these unique treasures. The spatial organization of the microbial colonizers and their relationships with the lithic substrate were analysed using scanning electron microscopy. This approach revealed extensive epilithic and endolithic colonization and close microbial–mineral interactions. Shotgun sequencing analysis revealed various taxa from the archaea, bacteria and some eukaryotes. Metagenomic coding sequences (CDS) of these microbial lithobionts exhibited specific metabolic pathways involved in the rock elements' cycles and uptake processes. Thus, our results provide evidence for the potential participation of the microorganisms colonizing these rocks during different solubilization and mineralization processes. These damaging actions may contribute to the deterioration of this extraordinary rock art and thus threaten this valuable heritage. Shotgun metagenomic sequencing, in conjunction with the in situ scanning electron microscopy study, can thus be considered an effective strategy to understand the complexity of the weathering processes occurring at petroglyph sites and other cultural heritage assets.     

The phylogeny of endolithic microbes associated with marine basalts

We examined the phylogenetic diversity of microbial communities associated with marine basalts, using over 300 publicly available 16S rDNA sequences and new sequence data from basalt enrichment cultures. Phylogenetic analysis provided support for 11 monophyletic clades originating from ocean crust (sediment, basalt and gabbro). Seven of the ocean crust clades (OCC) are bacterial, while the remaining four OCC are in the Marine Group I (MGI) Crenarchaeota. Most of the OCC were found at diverse geographic sites, suggesting that these microorganisms have cosmopolitan distributions. One OCC in the Crenarchaeota consisted of sequences derived entirely from basalts. The remaining OCC were found in both basalts and sediments. The MGI Crenarchaeota were observed in all studies where archaeal diversity was evaluated. These results demonstrate that basalts are occupied by cosmopolitan clades of microorganisms that are also found in marine sediments but are distinct from microorganisms found in other marine habitats, and that one OCC in the ubiquitous MGI Crenarchaeota clade may be an ecotype specifically adapted to basalt.     

First investigation of the microbiology of the deepest layer of ocean crust

The gabbroic layer comprises the majority of ocean crust. Opportunities to sample this expansive crustal environment are rare because of the technological demands of deep ocean drilling; thus, gabbroic microbial communities have not yet been studied. During the Integrated Ocean Drilling Program Expeditions 304 and 305, igneous rock samples were collected from 0.45-1391.01 meters below seafloor at Hole 1309D, located on the Atlantis Massif (30 °N, 42 °W). Microbial diversity in the rocks was analyzed by denaturing gradient gel electrophoresis and sequencing (Expedition 304), and terminal restriction fragment length polymorphism, cloning and sequencing, and functional gene microarray analysis (Expedition 305). The gabbroic microbial community was relatively depauperate, consisting of a low diversity of proteobacterial lineages closely related to Bacteria from hydrocarbon-dominated environments and to known hydrocarbon degraders, and there was little evidence of Archaea. Functional gene diversity in the gabbroic samples was analyzed with a microarray for metabolic genes ("GeoChip"), producing further evidence of genomic potential for hydrocarbon degradation--genes for aerobic methane and toluene oxidation. Genes coding for anaerobic respirations, such as nitrate reduction, sulfate reduction, and metal reduction, as well as genes for carbon fixation, nitrogen fixation, and ammonium-oxidation, were also present. Our results suggest that the gabbroic layer hosts a microbial community that can degrade hydrocarbons and fix carbon and nitrogen, and has the potential to employ a diversity of non-oxygen electron acceptors. This rare glimpse of the gabbroic ecosystem provides further support for the recent finding of hydrocarbons in deep ocean gabbro from Hole 1309D. It has been hypothesized that these hydrocarbons might originate abiotically from serpentinization reactions that are occurring deep in the Earth's crust, raising the possibility that the lithic microbial community reported here might utilize carbon sources produced independently of the surface biosphere.     

Extracellular enzymes in terrestrial, freshwater, and marine environments: perspectives on system variability and common research needs

Extracellular enzymes produced by heterotrophic microbial communities are major drivers of carbon and nutrient cycling in terrestrial, freshwater, and marine environments. Although carbon and nutrient cycles are coupled on global scales, studies of extracellular enzymes associated with terrestrial, freshwater, and marine microbial communities are not often compared across ecosystems. In part, this disconnect arises because the environmental parameters that control enzyme activities in terrestrial and freshwater systems, such as temperature, pH, and moisture content, have little explanatory power for patterns of enzyme activities in marine systems. Instead, factors such as the functional diversity of microbial communities may explain varying patterns of enzyme activities observed in the ocean to date. In any case, many studies across systems focus on similar issues that highlight the commonalities of microbial community organization. Examples include the effective lifetime of enzymes released into the environment; the extent to which microbial communities coordinate enzyme expression to decompose complex organic substrates; and the influence of microbial community composition on enzyme activities and kinetics. Here we review the often-disparate research foci in terrestrial, freshwater, and marine environments. We consider the extent to which environmental factors may regulate extracellular enzyme activities within each ecosystem, and highlight commonalities and current methodological challenges to identify research questions that may aid in integrating cross-system perspectives in the future.     

Tales from the tomb: the microbial ecology of exposed rock surfaces

Although a broad diversity of eukaryotic and bacterial taxa reside on rock surfaces where they can influence the weathering of rocks and minerals, these communities and their contributions to mineral weathering remain poorly resolved. To build a more comprehensive understanding of the diversity, ecology and potential functional attributes of microbial communities living on rock, we sampled 149 tombstones across three continents and analysed their bacterial and eukaryotic communities via marker gene and shotgun metagenomic sequencing. We found that geographic location and climate were important factors structuring the composition of these communities. Moreover, the tombstone‐associated microbial communities varied as a function of rock type, with granite and limestone tombstones from the same cemeteries harbouring taxonomically distinct microbial communities. The granite and limestone‐associated communities also had distinct functional attributes, with granite‐associated bacteria having more genes linked to acid tolerance and chemotaxis, while bacteria on limestone were more likely to be lichen associated and have genes involved in photosynthesis and radiation resistance. Together these results indicate that rock‐dwelling microbes exhibit adaptations to survive the stresses of the rock surface, differ based on location, climate and rock type, and seem pre‐disposed to different ecological strategies (symbiotic versus free‐living lifestyles) depending on the rock type.     

Silicates,Silicate Weathering,and Microbial Ecology

Mineralogy, microbial ecology, and mineral weathering in the subsurface are an intimately linked biogeochemical system. Although bacteria have been implicated indirectly in the accelerated weathering of minerals, it is not clear if this interaction is simply the coincidental result of microbial metabolism, or if it represents a specific strategy offering the colonizing bacteria a competitive ecological advantage. Our studies provide evidence that silicate weathering by bacteria is sometimes driven by the nutrient requirements of the microbial consortium, and therefore depends on the trace nutrient content of each aquifer mineral. This occurrence was observed in reducing groundwaters where carbon is abundant but phosphate is scarce; here, even resistant feldspars are weathered rapidly. This suggests that the progression of mineral weathering may be influenced by a mineral's nutritional potential, with microorganisms destroying only beneficial minerals. The rock record, therefore, may contain a remnant mineralogy that reflects early microbial destruction of biologically valuable minerals, leaving a residuum of "useless" minerals, where "value" depends on the organism, its metabolic needs, and the diagenetic environment. Conversely, the subsurface distribution of microorganisms may, in part, be controlled by the mineralogy and by the ability of an organism to take advantage of mineral-bound nutrients.     

Inorganic Species Distribution and Microbial Diversity within High Arctic Cryptoendolithic Habitats

Cryptoendolithic habitats in the Canadian high Arctic are associated with a variety of microbial community assemblages, including cyanobacteria, algae, and fungi. These habitats were analyzed for the presence of metal ions by sequential extraction and evaluated for relationships between these and the various microorganisms found at each site using multivariate statistical methods. Cyanobacteria-dominated communities exist under higher pH conditions with elevated concentrations of calcium and magnesium, whereas communities dominated by fungi and algae are characterized by lower pH conditions and higher concentrations of iron, aluminum, and silicon in the overlying surfaces. These results suggest that the activity of the dominant microorganisms controls the pH of the surrounding environment, which in turn dictates rates of weathering or the possibility for surface crust formation, both ultimately deciding the structure of microbial diversity for each cryptoendolithic habitat.     

Fungi as Geologic Agents

Although many studies on fungi and geological processes have been published in recent years, books and congress proceedings on geomicrobiology focus mainly on prokaryotes and algae. Therefore, it is the aim of this review to summarize data on the fungal impact on geological processes. These processes include the alteration and weathering of rock and minerals, the accumulation of metals, and the conversion of fossil organic carbon. Fossil records and fungi in subsurface environments are also discussed. This article especially emphasizes the role of epi- and endolithic black meristematic fungi, discussing their deteriorative potential on rock as well as their taxonomy and phylogeny. Moreover, the impact of fungi on weathering of monuments and building materials is described and new methods to study fungi-material interactions are presented. The data summarized here show that "geomycology" is a highly interesting discipline in view of basic geological research, as well as biotechnological application.     

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.     

河南卢氏和江西宜春两处锂矿山地表微生物群落分布特征差异及成因分析

[目的] 揭示地表锂矿石表面和风化产物中细菌群落多样性特征。[方法] 针对细菌16S rRNA片段扩增进行高通量测序,分析不同锂矿石表面及其风化产物中细菌群落组成、多样性及功能属性等信息。[结果] 河南卢氏南阳山伟晶岩型锂矿石和江西宜春花岗岩型锂矿石表面及其风化产物的细菌群落多样性有差异。南阳山伟晶岩矿石与其风化产物、宜春花岗岩矿石表面和风化产物（NK-1、NK-1F、YK-1、YK-1F、YK-2、YK-2F、YK-3）的OTUs分别是1010、540、835、828、1117、974和604,其差异与不同的矿物组成显著关联。两矿山均有其优势微生物,在门水平上,两矿山均以放线菌门（Actinobacteria）、变形菌门（Proteobacteria）为优势菌门。同时两矿区微生物群落组成具有显著差异性（P<0.05）,不同地理位置风化产物样本之间差异尤为显著（P<0.001）;在属水平上,NK-1中相对丰度大于5%的属为鞘氨醇单胞菌属（Sphingomonas）、马赛菌属（Massilia）;NK-1F为类芽孢杆菌属（Paenibacillus）、杆状细菌属（Bacillus）、马赛菌属（Massilia）;YK-1F为芽球菌属（Blastococcus）、念珠菌固体杆菌属（Candidatus-Solibacter）、Noviherbaspirillum属、伯克霍尔德氏菌属（Burkholderia-Caballeronia-Paraburkholderia）,YK-2为unidentified-Chloroplast属,YK-2F为北里孢菌属（Kitasatospora）,YK-3为1174-901-12属、甲基杆菌属（Methylobacterium）。不同地理位置的矿石及其风化物样本的功能注释均涉及代谢、遗传信息处理、环境信息处理等6个代谢通路。[结论] 16S rRNA高通量测序揭示不同地区锂矿石及其风化产物的细菌多样性存在差异,各具优势类群,样本间菌落组成、多样性及功能属性的差异与锂矿石化学组成、风化程度和地理分布密切相关。这项研究揭示了优势微生物类群的元素地球化学功能与含锂矿物地表风化的潜在联系,可为微生物生态分布研究及相关微生物资源开发提供新数据。