Summary
Subseafloor oceanic crust is a vast yet poorly sampled habitat for life. Recent studies suggest that microbial composition in crustal habitats is variable in space and time, but biogeographic ...patterns are difficult to determine due to a paucity of data. To address this, we deployed hundreds of mineral colonization experiments at and below the seafloor for 4–6 years at North Pond, a borehole observatory network in cool (<10°C) and oxic oceanic crust on the western flank of the Mid‐Atlantic Ridge. The overall community composition of mineral incubations reveals that colonization patterns are site dependent, with no correlation to mineral type. Only a few members of the Thioalkalispiraceae and Thioprofundaceae exhibited a mineral preference pattern, with generally higher abundance on metal sulphides compared to silicates, while taxa of the Gammaproteobacteria and Deltaproteobacteria were common in the colonization experiments. In comparison to datasets from other crustal habitats, broader biogeographic patterns of crustal communities emerge based on crustal habitat type (surface‐attached communities versus fluid communities), redox environment and possibly crustal age. These comparisons suggest successional biogeography patterning that might be used as an indicator of how recently permeable pathways were established within oceanic crust.
First reported in the 1960s, offshore freshened groundwater (OFG) has now been documented in most continental margins around the world. In this review we compile a database documenting OFG ...occurrences and analyze it to establish the general characteristics and controlling factors. We also assess methods used to map and characterize OFG, identify major knowledge gaps, and propose strategies to address them. OFG has a global volume of 1 × 106 km3; it predominantly occurs within 55 km of the coast and down to a water depth of 100 m. OFG is mainly hosted within siliciclastic aquifers on passive margins and recharged by meteoric water during Pleistocene sea level lowstands. Key factors influencing OFG distribution are topography‐driven flow, salinization via haline convection, permeability contrasts, and the continuity/connectivity of permeable and confining strata. Geochemical and stable isotope measurements of pore waters from boreholes have provided insights into OFG emplacement mechanisms, while recent advances in seismic reflection profiling, electromagnetic surveying, and numerical models have improved our understanding of OFG geometry and controls. Key knowledge gaps, such as the extent and function of OFG, and the timing of their emplacement, can be addressed by the application of isotopic age tracers, joint inversion of electromagnetic and seismic reflection data, and development of three‐dimensional hydrological models. We show that such advances, combined with site‐specific modeling, are necessary to assess the potential use of OFG as an unconventional source of water and its role in sub‐seafloor geomicrobiology.
Plain Language Summary
This review paper considers offshore freshened groundwater (OFG), which is water hosted in sediments and rocks below the seafloor, with a total dissolved solid concentration lower than seawater. We have compiled >300 records to demonstrate that freshened groundwater occurs offshore on most continents around the world and has a global volume of 1 × 106 km3. The majority of OFG was deposited when sea level was lower than today and is hosted in sandy sub‐seafloor layers that are located within 55 km of coasts in water depths less than 100 m. We present a range of geochemical, geophysical, and modeling approaches that have successfully been used to investigate OFG systems. We also propose approaches to address key scientific questions related to OFG, including whether it may be used as an unconventional source of potable water in coastal areas.
Key Points
Most known OFG is located at water depths of <100 m within 55 km of the coast, hosted in siliciclastic aquifers in passive margins
Key gaps in knowledge include the extent and function of OFG systems, as well as the mechanism and timing of emplacement
Isotopic tracers, jointly inverted geophysical data and 3‐D hydrological models can help address these knowledge gaps
Oxalate serves various functions in the biological processes of plants, fungi, bacteria, and animals. It occurs naturally in the minerals weddellite and whewellite (calcium oxalates) or as oxalic ...acid. The environmental accumulation of oxalate is disproportionately low compared to the prevalence of highly productive oxalogens, namely plants. It is hypothesized that oxalotrophic microbes limit oxalate accumulation by degrading oxalate minerals to carbonates via an under-explored biogeochemical cycle known as the oxalate-carbonate pathway (OCP). Neither the diversity nor the ecology of oxalotrophic bacteria is fully understood. This research investigated the phylogenetic relationships of the bacterial genes
,
,
, and
, which encode key enzymes for oxalotrophy, using bioinformatic approaches and publicly available omics datasets. Phylogenetic trees of
and
genes demonstrated grouping by both source environment and taxonomy. All four trees included genes from metagenome-assembled genomes (MAGs) that contained novel lineages and environments for oxalotrophs. In particular, sequences of each gene were recovered from marine environments. These results were supported with marine transcriptome sequences and description of key amino acid residue conservation. Additionally, we investigated the theoretical energy yield from oxalotrophy across marine-relevant pressure and temperature conditions and found similar standard state Gibbs free energy to "low energy" marine sediment metabolisms, such as anaerobic oxidation of methane coupled to sulfate reduction. These findings suggest further need to understand the role of bacterial oxalotrophy in the OCP, particularly in marine environments, and its contribution to global carbon cycling.
Biomineralization plays a fundamental role in the global silicon cycle. Grasses are known to mobilize significant quantities of Si in the form of silica biominerals and dominate the terrestrial realm ...today, but they have relatively recent origins and only rose to taxonomic and ecological prominence within the Cenozoic Era. This raises questions regarding when and how the biological silica cycle evolved. To address these questions, we examined silica abundances of extant members of early-diverging land plant clades, which show that silica biomineralization is widespread across terrestrial plant linages. Particularly high silica abundances are observed in lycophytes and early-diverging ferns. However, silica biomineralization is rare within later-evolving gymnosperms, implying a complex evolutionary history within the seed plants. Electron microscopy and X-ray spectroscopy show that the most common silica-mineralized tissues include the vascular system, epidermal cells, and stomata, which is consistent with the hypothesis that biomineralization in plants is frequently coupled to transpiration. Furthermore, sequence, phylogenetic, and structural analysis of nodulin 26-like intrinsic proteins from diverse plant genomes points to a plastic and ancient capacity for silica accumulation within terrestrial plants. The integration of these two comparative biology approaches demonstrates that silica biomineralization has been an important process for land plants over the course of their >400 My evolutionary history.
The past decade of scientific ocean drilling has revealed seemingly ubiquitous, slow-growing microbial life within a range of deep biosphere habitats. Integrated Ocean Drilling Program Expedition 337 ...expanded these studies by successfully coring Miocene-aged coal beds 2 km below the seafloor hypothesized to be “hot spots” for microbial life. To characterize the activity of coal-associated microorganisms from this site, a series of stable isotope probing (SIP) experiments were conducted using intact pieces of coal and overlying shale incubated at in situ temperatures (45 °C). The 30-month SIP incubations were amended with deuterated water as a passive tracer for growth and different combinations of 13C- or 15N-labeled methanol, methylamine, and ammonium added at low (micromolar) concentrations to investigate methylotrophy in the deep subseafloor biosphere. Although the cell densities were low (50–2,000 cells per cubic centimeter), bulk geochemical measurements and single-cell–targeted nanometer-scale secondary ion mass spectrometry demonstrated active metabolism of methylated substrates by the thermally adapted microbial assemblage, with differing substrate utilization profiles between coal and shale incubations. The conversion of labeled methylamine and methanol was predominantly through heterotrophic processes, with only minor stimulation of methanogenesis. These findings were consistent with in situ and incubation 16S rRNA gene surveys. Microbial growth estimates in the incubations ranged from several months to over 100 y, representing some of the slowest direct measurements of environmental microbial biosynthesis rates. Collectively, these data highlight a small, but viable, deep coal bed biosphere characterized by extremely slow-growing heterotrophs that can utilize a diverse range of carbon and nitrogen substrates.
The oceanic crustal aquifer is one of the largest habitable volumes on Earth, and it harbors a reservoir of microbial life that influences global-scale biogeochemical cycles. Here, we use time series ...metagenomic and metatranscriptomic data from a low-temperature, ridge flank environment representative of the majority of global hydrothermal fluid circulation in the ocean to reconstruct microbial metabolic potential, transcript abundance, and community dynamics. We also present metagenome-assembled genomes from recently collected fluids that are furthest removed from drilling disturbances. Our results suggest that the microbial community in the North Pond aquifer plays an important role in the oxidation of organic carbon within the crust. This community is motile and metabolically flexible, with the ability to use both autotrophic and organotrophic pathways, as well as function under low oxygen conditions by using alternative electron acceptors such as nitrate and thiosulfate. Anaerobic processes are most abundant in subseafloor horizons deepest in the aquifer, furthest from connectivity with the deep ocean, and there was little overlap in the active microbial populations between sampling horizons. This work highlights the heterogeneity of microbial life in the subseafloor aquifer and provides new insights into biogeochemical cycling in ocean crust.
Biogeochemical processes occurring in fluids that permeate oceanic crust make measurable contributions to the marine carbon cycle, but quantitative assessments of microbial impacts on this vast, ...subsurface carbon pool are lacking. We provide bulk and single-cell estimates of microbial biomass production from carbon and nitrogen substrates in cool, oxic basement fluids from the western flank of the Mid-Atlantic Ridge. The wide range in carbon and nitrogen incorporation rates indicates a microbial community well poised for dynamic conditions, potentially anabolizing carbon and nitrogen at rates ranging from those observed in subsurface sediments to those found in on-axis hydrothermal vent environments. Bicarbonate incorporation rates were highest where fluids are most isolated from recharging bottom seawater, suggesting that anabolism of inorganic carbon may be a potential strategy for supplementing the ancient and recalcitrant dissolved organic carbon that is prevalent in the globally distributed subseafloor crustal environment.
Chronic exposure to arsenic (As) by drinking shallow groundwater causes widespread disease in Bangladesh and neighboring countries. The release of As naturally present in sediment to groundwater has ...been linked to the reductive dissolution of iron oxides coupled to the microbial respiration of organic carbon (OC). The source of OC driving this microbial reduction—carbon deposited with the sediments or exogenous carbon transported by groundwater—is still debated despite its importance in regulating aquifer redox status and groundwater As levels. Here, we used the radiocarbon (¹⁴C) signature of microbial DNA isolated from groundwater samples to determine the relative importance of surface and sediment-derived OC. Three DNA samples collected from the shallow, high-As aquifer and one sample from the underlying, low-As aquifer were consistently younger than the total sediment carbon, by as much as several thousand years. This difference and the dominance of heterotrophic microorganisms implies that younger, surface-derived OC is advected within the aquifer, albeit more slowly than groundwater, and represents a critical pool of OC for aquifer microbial communities. The vertical profile shows that downward transport of dissolved OC is occurring on anthropogenic timescales, but bomb ¹⁴C-labeled dissolved OC has not yet accumulated in DNA and is not fueling reduction. These results indicate that advected OC controls aquifer redox status and confirm that As release is a natural process that predates human perturbations to groundwater flow. Anthropogenic perturbations, however, could affect groundwater redox conditions and As levels in the future.
Hot spring outflow channels provide geochemical gradients that are reflected in microbial community compositions. In many hot spring outflows, there is a distinct visual demarcation as the community ...transitions from predominantly chemotrophs to having visible pigments from phototrophs. It has been hypothesized that this transition to phototrophy, known as the photosynthetic fringe, is a result of the pH, temperature, and/or sulfide concentration gradients in the hot spring outflows. Here, we explicitly evaluated the predictive capability of geochemistry in determining the location of the photosynthetic fringe in hot spring outflows. A total of 46 samples were taken from 12 hot spring outflows in Yellowstone National Park that spanned pH values from 1.9 to 9.0 and temperatures from 28.9 to 92.2°C. Sampling locations were selected to be equidistant in geochemical space above and below the photosynthetic fringe based on linear discriminant analysis. Although pH, temperature, and total sulfide concentrations have all previously been cited as determining factors for microbial community composition, total sulfide did not correlate with microbial community composition with statistical significance in non-metric multidimensional scaling. In contrast, pH, temperature, ammonia, dissolved organic carbon, dissolved inorganic carbon, and dissolved oxygen did correlate with the microbial community composition with statistical significance. Additionally, there was observed statistical significance between beta diversity and the relative position to the photosynthetic fringe with sites above the photosynthetic fringe being significantly different from those at or below the photosynthetic fringe according to canonical correspondence analysis. However, in combination, the geochemical parameters considered in this study only accounted for 35% of the variation in microbial community composition determined by redundancy analysis. In co-occurrence network analyses, each clique correlated with either pH and/or temperature, whereas sulfide concentrations only correlated with individual nodes. These results indicate that there is a complex interplay between geochemical variables and the position of the photosynthetic fringe that cannot be fully explained by statistical correlations with the individual geochemical variables included in this study.
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