Tracking the Deep Biosphere through Time

A special issue of Geosciences (ISSN 2076-3263). This special issue belongs to the section "Biogeosciences".

Deadline for manuscript submissions: closed (1 December 2019) | Viewed by 30373

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Special Issue Editors


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Guest Editor
Department of Biology and Environmental Science, Linnaeus University, Kalmar, Sweden
Interests: isotope geochemistry; deep biosphere; geobiology; deep time; geochronology; greenhouse gases

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Guest Editor
1. Department of Biology, University of Southern Denmark, Campusvej 55, 5230 Odense, Denmark
2. Department of Paleobiology, Swedish Museum of Natural History, Frescativägen 40, 114 18 Stockholm, Sweden
Interests: deep biosphere; geobiology; paleobiology; fossilized microorganisms
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Guest Editor
Department of Geobiology, Geoscience Centre, University of Göttingen, Göttingen, Germany
Interests: recent and ancient ecosystems in the deep biosphere; biosignatures and microbial mats in extreme environments

Special Issue Information

Dear Colleagues,

The oceanic and continental lithosphere constitutes Earth´s largest microbial habitat, yet it is poorly investigated and not well understood. Its physical and chemical properties are distinctly different from the overlaying soils and the hydrosphere, which greatly impacts the microbial communities and associated geobiological and geochemical processes. Fluid-rock interactions, i.e., the serpentinization of ultramafic rocks and the subsequent production of gases and molecular species, are key processes for microbial colonization and persistence in a nutrient-poor and extreme environment. Investigations during recent years have indicated microorganism-related processes, stable isotope variations, and species that are unique to the subsurface crust. Recent advances in geochronology have enabled the direct dating of minerals formed in response to microbial activity, which in turn have led to an increasing understanding of the evolution of the deep biosphere in (deep) time. Similarly, the preservation of isotopic signatures as well as organic compounds within fossilized microcolonies or related mineral assemblages in voids, cements, and fractures/veins in the upper crust provide an archive that can be tapped for knowledge about ancient microbial activity, including both prokaryotic and eukaryotic life. This knowledge sheds light on how lifeforms have evolved in the energy-poor subsurface, but also contributes to the understanding of the boundaries of life on Earth, of early Earth life at times when the surface was inhabitible, and of the preservation of signatures of ancient life, which may have astrobiological implications.

This Special Issue seeks to cover all geobiological aspects of the upper crust (continental and marine) and we invite contributions with relevance to geomicrobiology, isotope geochemistry, microbial-activity-associated geochronology and related geochemical and hydrochemical proxies as well as presentations on new methods, techniques, and experimental approaches in both the modern and ancient crust. We wish to cover a broad spectrum of environments such as ultra-mafic, mafic, and felsic systems, as well as hydrothermal/geothermal areas and sedimentary successions. We encourage contributions related to scientific drilling programs as well as research from underground facilites and deep drillings related to mining activity or nuclear waste disposal, in addition to studies of exposed ancient crust. Astrobiological implications are also encouraged.

Dr. Henrik Drake
Dr. Magnus Ivarsson
Dr. Christine Heim
Guest Editors

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Keywords

  • deep biosphere
  • geobiology
  • deep time
  • geochronology
  • microorganisms
  • evolution

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Published Papers (8 papers)

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Editorial

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6 pages, 215 KiB  
Editorial
Tracking the Deep Biosphere through Time
by Henrik Drake, Magnus Ivarsson and Christine Heim
Geosciences 2020, 10(11), 461; https://doi.org/10.3390/geosciences10110461 - 15 Nov 2020
Cited by 2 | Viewed by 2154
Abstract
The oceanic and continental lithosphere constitutes Earth’s largest microbial habitat, yet it is scarcely investigated and not well understood. The physical and chemical properties here are distinctly different from the overlaying soils and the hydrosphere, which greatly impact the microbial communities and associated [...] Read more.
The oceanic and continental lithosphere constitutes Earth’s largest microbial habitat, yet it is scarcely investigated and not well understood. The physical and chemical properties here are distinctly different from the overlaying soils and the hydrosphere, which greatly impact the microbial communities and associated geobiological and geochemical processes. Fluid–rock interactions are key processes for microbial colonization and persistence in a nutrient-poor and extreme environment. Investigations during recent years have spotted microbial processes, stable isotope variations, and species that are unique to the subsurface crust. Recent advances in geochronology have enabled the direct dating of minerals formed in response to microbial activity, which in turn have led to an increased understanding of the evolution of the deep biosphere in (deep) time. Similarly, the preservation of isotopic signatures, as well as organic compounds within fossilized micro-colonies or related mineral assemblages in voids, cements, and fractures/veins in the upper crust, provides an archive that can be tapped for knowledge about ancient microbial activity, including both prokaryotic and eukaryotic life. This knowledge sheds light on how lifeforms have evolved in the energy-poor subsurface, but also contributes to the understanding of the boundaries of life on Earth, of early life when the surface was not habitable, and of the preservation of signatures of ancient life, which may have astrobiological implications. The Special Issue “Tracking the Deep Biosphere through Time” presents a collection of scientific contributions that provide a sample of forefront research in this field. The contributions involve a range of case studies of deep ancient life in continental and oceanic settings, of microbial diversity in sub-seafloor environments, of isolation of calcifying bacteria as well as reviews of clay mineralization of fungal biofilms and of the carbon isotope records of the deep biosphere. Full article
(This article belongs to the Special Issue Tracking the Deep Biosphere through Time)

Research

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17 pages, 3851 KiB  
Article
Geochronology and Stable Isotope Analysis of Fracture-Fill and Karst Mineralization Reveal Sub-Surface Paleo-Fluid Flow and Microbial Activity of the COSC-1 Borehole, Scandinavian Caledonides
by Henrik Drake, Nick M. W. Roberts and Martin J. Whitehouse
Geosciences 2020, 10(2), 56; https://doi.org/10.3390/geosciences10020056 - 03 Feb 2020
Cited by 9 | Viewed by 3608
Abstract
The deep biosphere hosted in fractured rocks within the upper continental crust is one of the least understood and studied ecological realms on Earth. Scarce knowledge of ancient life and paleo-fluid flow within this realm is owing to the lack of deep drilling [...] Read more.
The deep biosphere hosted in fractured rocks within the upper continental crust is one of the least understood and studied ecological realms on Earth. Scarce knowledge of ancient life and paleo-fluid flow within this realm is owing to the lack of deep drilling into the crust. Here we apply microscale high spatial-resolution analytical techniques to fine-grained secondary minerals in a deep borehole (COSC-1) drilled into the Silurian-Devonian Scandinavian Caledonide mountain range in central Sweden. The aim is to detect and date signs of ancient microbial activity and low-temperature fluid circulation in micro-karsts (foliation-parallel dissolution cavities in the rock) and fractures at depth in the nappe system. Vein carbonates sampled at 684 to 2210 m show a decreased C isotope variability at depths below 1050 m; likely due to decreased influence of organic-C at great depth. Micro-karsts at 122–178 m depth feature at least two generations of secondary calcite and pyrite growth in the voids as shown by secondary ion mass spectrometry analytical transects within individual grains. The younger of these two precipitation phases shows 34S-depleted δ34Spyrite values (−19.8 ± 1.6‰ vs. Vienna-Canyon Diablo Troilite (V-CDT)) suggesting microbial sulfate reduction in situ. The calcite of this late phase can be distinguished from the older calcite by higher δ18Ocalcite values that correspond to precipitation from ambient meteoric water. The late stage calcite gave two separate laser ablation inductively coupled mass spectrometry-derived U-Pb ages (9.6 ± 1.3 Ma and 2.5 ± 0.2 Ma), marking a minimum age for widespread micro-karst formation within the nappe. Several stages of fluid flow and mineral precipitation followed karst formation; with related bacterial activity as late as the Neogene-Quaternary; in structures presently water conducting. The results show that our combined high spatial-resolution stable isotope and geochronology approach is suitable for characterizing paleo-fluid flow in micro-karst; in this case, of the crystalline crust comprising orogenic nappe units. Full article
(This article belongs to the Special Issue Tracking the Deep Biosphere through Time)
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26 pages, 7455 KiB  
Article
A Novel Approach to Isolation and Screening of Calcifying Bacteria for Biotechnological Applications
by Paola Cacchio and Maddalena Del Gallo
Geosciences 2019, 9(11), 479; https://doi.org/10.3390/geosciences9110479 - 14 Nov 2019
Cited by 10 | Viewed by 3683
Abstract
Bacterial calcium-carbonate precipitation (BCP) has been studied for multiple applications such as remediation, consolidation, and cementation. Isolation and screening of strong calcifying bacteria is the main task of BCP-technique. In this paper, we studied CaCO3 precipitation by different bacteria isolated from a [...] Read more.
Bacterial calcium-carbonate precipitation (BCP) has been studied for multiple applications such as remediation, consolidation, and cementation. Isolation and screening of strong calcifying bacteria is the main task of BCP-technique. In this paper, we studied CaCO3 precipitation by different bacteria isolated from a rhizospheric soil in both solid and liquid media. It has been found, through culture-depending studies, that bacteria belonging to Actinobacteria, Gammaproteobacteria, and Alphaproteobacteria are the dominant bacteria involved in CaCO3 precipitation in this environment. Pure and mixed cultures of selected strains were applied for sand biocementation experiments. Scanning electron microscopy (SEM) and energy dispersive X-ray spectroscopy (EDS) analyses of the biotreated samples revealed the biological nature of the cementation and the effectiveness of the biodeposition treatment by mixed cultures. X-ray diffraction (XRD) analysis confirmed that all the calcifying strains selected for sand biocementation precipitated CaCO3, mostly in the form of calcite. In this study, Biolog® EcoPlate is evaluated as a useful method for a more targeted choice of the sampling site with the purpose of obtaining interesting candidates for BCP applications. Furthermore, ImageJ software was investigated, for the first time to our knowledge, as a potential method to screen high CaCO3 producer strains. Full article
(This article belongs to the Special Issue Tracking the Deep Biosphere through Time)
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20 pages, 4149 KiB  
Article
Fossilized Endolithic Microorganisms in Pillow Lavas from the Troodos Ophiolite, Cyprus
by Diana-Thean Carlsson, Magnus Ivarsson and Anna Neubeck
Geosciences 2019, 9(11), 456; https://doi.org/10.3390/geosciences9110456 - 23 Oct 2019
Cited by 5 | Viewed by 2987
Abstract
The last decade has revealed the igneous oceanic crust to host a more abundant and diverse biota than previously expected. These underexplored rock-hosted deep ecosystems dominated Earth’s biosphere prior to plants colonized land in the Ordovician, thus the fossil record of deep endoliths [...] Read more.
The last decade has revealed the igneous oceanic crust to host a more abundant and diverse biota than previously expected. These underexplored rock-hosted deep ecosystems dominated Earth’s biosphere prior to plants colonized land in the Ordovician, thus the fossil record of deep endoliths holds invaluable clues to early life and the work to decrypt them needs to be intensified. Here, we present fossilized microorganisms found in open and sealed pore spaces in pillow lavas from the Troodos Ophiolite (91 Ma) on Cyprus. A fungal interpretation is inferred upon the microorganisms based on characteristic morphological features. Geochemical conditions are reconstructed using data from mineralogy, fluid inclusions and the fossils themselves. Mineralogy indicates at least three hydrothermal events and a continuous increase of temperature and pH. Precipitation of 1) celadonite and saponite together with the microbial introduction was followed by 2) Na and Ca zeolites resulting in clay adherence on the microorganisms as protection, and finally 3) Ca carbonates resulted in final fossilization and preservation of the organisms in-situ. Deciphering the fossil record of the deep subseafloor biosphere is a challenging task, but when successful, can unlock doors to life’s cryptic past. Full article
(This article belongs to the Special Issue Tracking the Deep Biosphere through Time)
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18 pages, 1588 KiB  
Article
Microbial Diversity in Sub-Seafloor Sediments from the Costa Rica Margin
by Amanda Martino, Matthew E. Rhodes, Rosa León-Zayas, Isabella E. Valente, Jennifer F. Biddle and Christopher H. House
Geosciences 2019, 9(5), 218; https://doi.org/10.3390/geosciences9050218 - 13 May 2019
Cited by 10 | Viewed by 4709
Abstract
The exploration of the deep biosphere continues to reveal a great diversity of microorganisms, many of which remain poorly understood. This study provides a first look at the microbial community composition of the Costa Rica Margin sub-seafloor from two sites on the upper [...] Read more.
The exploration of the deep biosphere continues to reveal a great diversity of microorganisms, many of which remain poorly understood. This study provides a first look at the microbial community composition of the Costa Rica Margin sub-seafloor from two sites on the upper plate of the subduction zone, between the Cocos and Caribbean plates. Despite being in close geographical proximity, with similar lithologies, both sites show distinctions in the relative abundance of the archaeal domain and major microbial phyla, assessed using a pair of universal primers and supported by the sequencing of six metagenomes. Elusimicrobia, Chloroflexi, Aerophobetes, Actinobacteria, Lokiarchaeota, and Atribacteria were dominant phyla at Site 1378, and Bathyarchaeota, Chloroflexi, Hadesarchaeota, Aerophobetes, Elusimicrobia, and Lokiarchaeota were dominant at Site 1379. Correlations of microbial taxa with geochemistry were examined and notable relationships were seen with ammonia, sulfate, and depth. With deep sediments, there is always a concern that drilling technologies impact analyses due to contamination of the sediments via drilling fluid. Here, we use analysis of the drilling fluid in conjunction with the sediment analysis, to assess the level of contamination and remove any problematic sequences. In the majority of samples, we find the level of drilling fluid contamination, negligible. Full article
(This article belongs to the Special Issue Tracking the Deep Biosphere through Time)
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22 pages, 2296 KiB  
Article
Re-Evaluating the Age of Deep Biosphere Fossils in the Lockne Impact Structure
by Mikael Tillberg, Magnus Ivarsson, Henrik Drake, Martin J. Whitehouse, Ellen Kooijman and Melanie Schmitt
Geosciences 2019, 9(5), 202; https://doi.org/10.3390/geosciences9050202 - 07 May 2019
Cited by 7 | Viewed by 3276
Abstract
Impact-generated hydrothermal systems have been suggested as favourable environments for deep microbial ecosystems on Earth, and possibly beyond. Fossil evidence from a handful of impact craters worldwide have been used to support this notion. However, as always with mineralized remains of microorganisms in [...] Read more.
Impact-generated hydrothermal systems have been suggested as favourable environments for deep microbial ecosystems on Earth, and possibly beyond. Fossil evidence from a handful of impact craters worldwide have been used to support this notion. However, as always with mineralized remains of microorganisms in crystalline rock, certain time constraints with respect to the ecosystems and their subsequent fossilization are difficult to obtain. Here we re-evaluate previously described fungal fossils from the Lockne crater (458 Ma), Sweden. Based on in-situ Rb/Sr dating of secondary calcite-albite-feldspar (356.6 ± 6.7 Ma) we conclude that the fungal colonization took place at least 100 Myr after the impact event, thus long after the impact-induced hydrothermal activity ceased. We also present microscale stable isotope data of 13C-enriched calcite suggesting the presence of methanogens contemporary with the fungi. Thus, the Lockne fungi fossils are not, as previously thought, related to the impact event, but nevertheless have colonized fractures that may have been formed or were reactivated by the impact. Instead, the Lockne fossils show similar features as recent findings of ancient microbial remains elsewhere in the fractured Swedish Precambrian basement and may thus represent a more general feature in this scarcely explored habitat than previously known. Full article
(This article belongs to the Special Issue Tracking the Deep Biosphere through Time)
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Review

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25 pages, 2696 KiB  
Review
The Carbon-Isotope Record of the Sub-Seafloor Biosphere
by Patrick Meister and Carolina Reyes
Geosciences 2019, 9(12), 507; https://doi.org/10.3390/geosciences9120507 - 05 Dec 2019
Cited by 21 | Viewed by 5344
Abstract
Sub-seafloor microbial environments exhibit large carbon-isotope fractionation effects as a result of microbial enzymatic reactions. Isotopically light, dissolved inorganic carbon (DIC) derived from organic carbon is commonly released into the interstitial water due to microbial dissimilatory processes prevailing in the sub-surface biosphere. Much [...] Read more.
Sub-seafloor microbial environments exhibit large carbon-isotope fractionation effects as a result of microbial enzymatic reactions. Isotopically light, dissolved inorganic carbon (DIC) derived from organic carbon is commonly released into the interstitial water due to microbial dissimilatory processes prevailing in the sub-surface biosphere. Much stronger carbon-isotope fractionation occurs, however, during methanogenesis, whereby methane is depleted in 13C and, by mass balance, DIC is enriched in 13C, such that isotopic distributions are predominantly influenced by microbial metabolisms involving methane. Methane metabolisms are essentially mediated through a single enzymatic pathway in both Archaea and Bacteria, the Wood–Ljungdahl (WL) pathway, but it remains unclear where in the pathway carbon-isotope fractionation occurs. While it is generally assumed that fractionation arises from kinetic effects of enzymatic reactions, it has recently been suggested that partial carbon-isotope equilibration occurs within the pathway of anaerobic methane oxidation. Equilibrium fractionation might also occur during methanogenesis, as the isotopic difference between DIC and methane is commonly on the order of 75‰, which is near the thermodynamic equilibrium. The isotopic signature in DIC and methane highly varies in marine porewaters, reflecting the distribution of different microbial metabolisms contributing to DIC. If carbon isotopes are preserved in diagenetic carbonates, they may provide a powerful biosignature for the conditions in the deep biosphere, specifically in proximity to the sulphate–methane transition zone. Large variations in isotopic signatures in diagenetic archives have been found that document dramatic changes in sub-seafloor biosphere activity over geological time scales. We present a brief overview on carbon isotopes, including microbial fractionation mechanisms, transport effects, preservation in diagenetic carbonate archives, and their implications for the past sub-seafloor biosphere and its role in the global carbon cycle. We discuss open questions and future potentials of carbon isotopes as archives to trace the deep biosphere through time. Full article
(This article belongs to the Special Issue Tracking the Deep Biosphere through Time)
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21 pages, 5146 KiB  
Review
Instant Attraction: Clay Authigenesis in Fossil Fungal Biofilms
by Therese Sallstedt, Magnus Ivarsson, Henrik Drake and Henrik Skogby
Geosciences 2019, 9(9), 369; https://doi.org/10.3390/geosciences9090369 - 24 Aug 2019
Cited by 7 | Viewed by 3561
Abstract
Clay authigenesis associated with the activity of microorganisms is an important process for biofilm preservation and may provide clues to the formation of biominerals on the ancient Earth. Fossilization of fungal biofilms attached to vesicles or cracks in igneous rock, is characterized by [...] Read more.
Clay authigenesis associated with the activity of microorganisms is an important process for biofilm preservation and may provide clues to the formation of biominerals on the ancient Earth. Fossilization of fungal biofilms attached to vesicles or cracks in igneous rock, is characterized by fungal-induced clay mineralization and can be tracked in deep rock and deep time, from late Paleoproterozoic (2.4 Ga), to the present. Here we briefly review the current data on clay mineralization by fossil fungal biofilms from oceanic and continental subsurface igneous rock. The aim of this study was to compare the nature of subsurface fungal clays from different igneous settings to evaluate the importance of host rock and ambient redox conditions for clay speciation related to fossil microorganisms. Our study suggests that the most common type of authigenic clay associated with pristine fossil fungal biofilms in both oxic (basaltic) and anoxic (granitic) settings are montmorillonite-like smectites and confirms a significant role of fungal biofilms in the cycling of elements between host rock, ocean and secondary precipitates. The presence of life in the deep subsurface may thus prove more significant than host rock geochemistry in directing the precipitation of authigenic clays in the igneous crust, the extent of which remains to be fully understood. Full article
(This article belongs to the Special Issue Tracking the Deep Biosphere through Time)
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