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Colonization of subsurface microbial observatories deployed in young ocean crust.

ABSTRACT: Oceanic crust comprises the largest hydrogeologic reservoir on Earth, containing fluids in thermodynamic disequilibrium with the basaltic crust. Little is known about microbial ecosystems that inhabit this vast realm and exploit chemically favorable conditions for metabolic activities. Crustal samples recovered from ocean drilling operations are often compromised for microbiological assays, hampering efforts to resolve the extent and functioning of a subsurface biosphere. We report results from the first in situ experimental observatory systems that have been used to study subseafloor life. Experiments deployed for 4 years in young (3.5?Ma) basaltic crust on the eastern flank of the Juan de Fuca Ridge record a dynamic, post-drilling response of crustal microbial ecosystems to changing physical and chemical conditions. Twisted stalks exhibiting a biogenic iron oxyhydroxide signature coated the surface of mineral substrates in the observatories; these are biosignatures indicating colonization by iron oxidizing bacteria during an initial phase of cool, oxic, iron-rich conditions following observatory installation. Following thermal and chemical recovery to warmer, reducing conditions, the in situ microbial structure in the observatory shifted, becoming representative of natural conditions in regional crustal fluids. Firmicutes, metabolic potential of which is unknown but may involve N or S cycling, dominated the post-rebound bacterial community. The archaeal community exhibited an extremely low diversity. Our experiment documented in situ conditions within a natural hydrological system that can pervade over millennia, exemplifying the power of observatory experiments for exploring the subsurface basaltic biosphere, the largest but most poorly understood biotope on Earth.

SUBMITTER: Orcutt BN

PROVIDER: S-EPMC3217339 | biostudies-literature | 2011 Apr

REPOSITORIES: biostudies-literature

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Colonization of subsurface microbial observatories deployed in young ocean crust.

Orcutt Beth N BN Bach Wolfgang W Becker Keir K Fisher Andrew T AT Hentscher Michael M Toner Brandy M BM Wheat C Geoffrey CG Edwards Katrina J KJ

The ISME journal 20101125 4

Oceanic crust comprises the largest hydrogeologic reservoir on Earth, containing fluids in thermodynamic disequilibrium with the basaltic crust. Little is known about microbial ecosystems that inhabit this vast realm and exploit chemically favorable conditions for metabolic activities. Crustal samples recovered from ocean drilling operations are often compromised for microbiological assays, hampering efforts to resolve the extent and functioning of a subsurface biosphere. We report results from ...[more]

PMID: 21107442

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Project description:One of the most promising planetary bodies that might harbor extraterrestrial life is Mars, given the presence of liquid water in the deep subsurface. The upper crust of Mars is mainly composed of >3.7-billion-year-old basaltic lava where heat-driven fluid circulation is negligible. The analogous crustal environment to the Martian subsurface is found in the Earth's oceanic crust composed of basaltic lava. The basaltic crust tends to cool down for 10-20-million-years after formation. However, microbial life in old cold basaltic lava is largely unknown even in the Earth's oceanic crust, because the lack of vigorous circulation prevents sampling of pristine crustal fluid from boreholes. Alternatively, it is important to investigate deep microbial life using pristine drill cores obtained from basaltic lava. We investigated a basaltic rock core sample with mineral-filled fractures drilled during Integral Ocean Drilling Project Expedition 329 that targeted 104-million-year-old oceanic crust. Mineralogical characterizations of fracture-infilling minerals revealed that fractures/veins were filled with Mg-rich smectite called saponite and calcium carbonate. The organic carbon content from the saponite-rich clay fraction in the core sample was 23 times higher than that from the bulk counterpart, which appears to be sufficient to supply energy and carbon sources to saponite-hosted life. Furthermore, a newly developed method to detect microbial cells in a thin-section of the saponite-bearing fracture revealed the dense colonization of SYBR-Green-I stained microbial cells spatially associated with saponite. These results suggest that the presence of saponite in old cold basaltic crust is favorable for microbial life. In addition to carbonaceous chondrite, saponite is a common product of low-temperature reactions between water and mafic minerals on Earth and Mars. It is therefore expected that deep saponite-bearing fractures could host extant life and/or the past life on Mars.

Project description:This study employed 16S rRNA gene amplicon pyrosequencing to examine the hypothesis that chemolithotrophic Fe(II)-oxidizing bacteria (FeOB) would preferentially colonize the Fe(II)-bearing mineral biotite compared to quartz sand when the minerals were incubated in situ within a subsurface redox transition zone (RTZ) at the Hanford 300 Area site in Richland, WA, USA. The work was motivated by the recently documented presence of neutral-pH chemolithotrophic FeOB capable of oxidizing structural Fe(II) in primary silicate and secondary phyllosilicate minerals in 300 Area sediments and groundwater (Benzine et al., 2013). Sterilized portions of sand+biotite or sand alone were incubated in situ for 5 months within a multilevel sampling (MLS) apparatus that spanned a ca. 2-m interval across the RTZ in two separate groundwater wells. Parallel MLS measurements of aqueous geochemical species were performed prior to deployment of the minerals. Contrary to expectations, the 16S rRNA gene libraries showed no significant difference in microbial communities that colonized the sand+biotite vs. sand-only deployments. Both mineral-associated and groundwater communities were dominated by heterotrophic taxa, with organisms from the Pseudomonadaceae accounting for up to 70% of all reads from the colonized minerals. These results are consistent with previous results indicating the capacity for heterotrophic metabolism (including anaerobic metabolism below the RTZ) as well as the predominance of heterotrophic taxa within 300 Area sediments and groundwater. Although heterotrophic organisms clearly dominated the colonized minerals, several putative lithotrophic (NH4 (+), H2, Fe(II), and HS(-) oxidizing) taxa were detected in significant abundance above and within the RTZ. Such organisms may play a role in the coupling of anaerobic microbial metabolism to oxidative pathways with attendant impacts on elemental cycling and redox-sensitive contaminant behavior in the vicinity of the RTZ.

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Dataset Information

Colonization of subsurface microbial observatories deployed in young ocean crust.

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Colonization of subsurface microbial observatories deployed in young ocean crust.

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