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Title: Meta‐omics highlights the diversity, activity and adaptations of fungi in deep oceanic crust
Summary

The lithified oceanic crust, lower crust gabbros in particular, has remained largely unexplored by microbiologists. Recently, evidence for heterogeneously distributed viable and transcriptionally active autotrophic and heterotrophic microbial populations within low‐biomass communities was found down to 750 m below the seafloor at the Atlantis Bank Gabbro Massif, Indian Ocean. Here, we report on the diversity, activity and adaptations of fungal communities in the deep oceanic crust from ~10 to 780 mbsf by combining metabarcoding analyses with mid/high‐throughput culturing approaches. Metabarcoding along with culturing indicate a low diversity of viable fungi, mostly affiliated to ubiquitous (terrestrial and aquatic environments) taxa. Ecophysiological analyses coupled with metatranscriptomics point to viable and transcriptionally active fungal populations engaged in cell division, translation, protein modifications and other vital cellular processes. Transcript data suggest possible adaptations for surviving in the nutrient‐poor, lithified deep biosphere that include the recycling of organic matter. These active communities appear strongly influenced by the presence of cracks and veins in the rocks where fluids and resulting rock alteration create micro‐niches.

 
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Award ID(s):
1658118
NSF-PAR ID:
10453921
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Environmental Microbiology
Volume:
22
Issue:
9
ISSN:
1462-2912
Page Range / eLocation ID:
p. 3950-3967
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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  5. null (Ed.)
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Their positions adjacent to or atop fault scarps on the forearc are likely related to the regional extension and vertical tectonic deformation in the forearc. Serpentinite mudflows at these volcanoes include serpentinized forearc mantle clasts, crustal and subducted Pacific plate materials, a matrix of serpentinite muds, and deep-sourced formation fluid. Mud volcanism on the Mariana forearc occurs within 100 km of the trench, representing a range of depths and temperatures to the downgoing plate and the subduction channel. These processes have likely been active for tens of millions of years at this site and for billions of years on Earth. At least 10 active serpentinite mud volcanoes have been located in the Mariana forearc. Two of these mud volcanoes are Conical and South Chamorro Seamounts, which are the furthest from the Mariana Trench at 86 and 78 km, respectively. Both seamounts were cored during Ocean Drilling Program (ODP) Legs 125 and 195, respectively. Data from these two seamounts represent deeper, warmer examples of the continuum of slab-derived materials as the Pacific plate subducts, providing a snapshot of how slab subduction affects fluid release, the composition of ascending fluids, mantle hydration, and the metamorphic paragenesis of subducted oceanic lithosphere. Data from the study of these two mud volcanoes constrain the pressure, temperature, and composition of fluids and materials within the subduction channel at depths of about 18 to 19 km. Understanding such processes is necessary for elucidating factors that control seismicity in convergent margins, tectonic and magma genesis processes in the forearc and volcanic arc, fluid and material fluxes, and the nature and variability of environmental conditions that impact subseafloor microbial communities. Expedition 366 centered on data collection from cores recovered from three serpentinite mud volcanoes that define a continuum of subduction-channel processes defined by the two previously cored serpentinite mud volcanoes and the trench. Three serpentinite mud volcanoes (Yinazao, Fantangisña, and Asùt Tesoro) were chosen at distances 55 to 72 km from the Mariana Trench. Cores were recovered from active sites of eruption on their summit regions and on the flanks where ancient flows are overlain by more recent ones. Recovered materials show the effects of dynamic processes that are active at these sites, bringing a range of materials to the seafloor, including materials from the lithosphere of the Pacific plate and from subducted seamounts (including corals). Most of the recovered material consists of serpentinite mud containing lithic clasts, which are derived from the underlying forearc crust and mantle and the subducting Pacific plate. Cores from each of the three seamounts drilled during Expedition 366, as well as those from Legs 125 and 195, include material from the underlying Pacific plate. A thin cover of pelagic sediment was recovered at many Expedition 366 sites, and at Site U1498 we cored through serpentinite flows to the underlying pelagic sediment and volcanic ash deposits. Recovered serpentinites are largely uniform in major element composition, with serpentinized ultramafic rocks and serpentinite muds spanning a limited range in SiO2 , MgO, and Fe2 O3 compositions. However, variation in trace element composition reflects pore fluid composition, which differs as a function of the temperature and pressure of the underlying subduction channel. Dissolved gases H2 , CH4 , and C2 H6 are highest at the site furthest from the trench, which also has the most active fluid discharge of the Expedition 366 serpentinite mud volcanoes. These dissolved gases and their active discharge from depth likely support active microbial communities, which were the focus of in-depth subsampling and preservation for shore-based analytical and culturing procedures. The effects of fluid discharge were also registered in the porosity and GRA density data indicated by higher than expected values at some of the summit sites. These higher values are consistent with overpressured fluids that minimize compaction of serpentinite mud deposits. In contrast, flank sites have significantly greater decreases in porosity with depth, suggesting that processes in addition to compaction are required to achieve the observed data. Thermal measurements reveal higher heat flow values on the flanks (~31 mW/m2) than on the summits (~17 mW/m2) of the seamounts. The new 2G Enterprises superconducting rock magnetometer (liquid helium free) revealed relatively high values of both magnetization and bulk magnetic susceptibility of discrete samples related to ultramafic rocks, particularly in dunite. Magnetite, a product of serpentinization, and authigenic carbonates were observed in the mudflow matrix materials. In addition to coring operations, Expedition 366 focused on the deployment and remediation of borehole casings for future observatories and set the framework for in situ experimentation. Borehole work commenced at South Chamorro Seamount, where the original-style CORK was partially removed. Work then continued at each of the three summit sites following coring operations. Cased boreholes with at least three joints of screened casing were deployed, and a plug of cement was placed at the bottom of each hole. Water samples were collected from two of the three boreholes, revealing significant inputs of formation fluids. This suggests that each of the boreholes tapped a hydrologic zone, making these boreholes suitable for experimentation with the future deployment of a CORK-lite. An active education and outreach program connected with many classrooms on shore and with the general public through social media. 
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