Recycling and metabolic flexibility dictate life in the lower oceanic crust
Authors: Donna K Blackman
Jiangtao Li
Frieder Klein
David Beaudoin
Paraskevi Mara
Jason B Sylvan
Shu Ying Wee
Sarah Lott
Florence Schubotz
Ga√´tan Burgaud
Rebecca Cox
Virginia P Edgcomb
Henry J B Dick
Maxence Qu√©mener
Lara A E Meyer
Journal: Nature (2020)
Discipline: Multidisciplinary
Keywords: lower oceanic crust; microbiota; carbon resources; energy; survival strategies
Affiliations: State Key Laboratory of Marine Geology, Tongji University, Shanghai, China., Department of Geology and Geophysics, Woods Hole Oceanographic Institution, Woods Hole, MA, USA., MARUM, University of Bremen, Bremen, Germany., Department of Geosciences, University of Bremen, Bremen, Germany., Department of Oceanography, Texas A&M University, College Station, TX, USA., Universit√© de Brest, EA 3882, Laboratoire Universitaire de Biodiversit√© et Ecologie Microbienne, ESIAB, Technop√¥le Brest-Iroise, Plouzan√©, France., Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA., Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA, USA., Department of Geology and Geophysics, Woods Hole Oceanographic Institution, Woods Hole, MA, USA. .

Abstract:  The lithified lower oceanic crust is one of Earth's last biological frontiers as it is difficult to access. It is challenging for microbiota that live in marine subsurface sediments or igneous basement to obtain sufficient carbon resources and energy to support growth1-3 or to meet basal power requirements4 during periods of resource scarcity. Here we show how limited and unpredictable sources of carbon and energy dictate survival strategies used by low-biomass microbial communities that live 10-750 m below the seafloor at Atlantis Bank, Indian Ocean, where Earth's lower crust is exposed at the seafloor. Assays of enzyme activities, lipid biomarkers, marker genes and microscopy indicate heterogeneously distributed and viable biomass with ultralow cell densities (fewer than 2,000 cells per cm3). Expression of genes involved in unexpected heterotrophic processes includes those with a role in the degradation of polyaromatic hydrocarbons, use of polyhydroxyalkanoates as carbon-storage molecules and recycling of amino acids to produce compounds that can participate in redox reactions and energy production. Our study provides insights into how microorganisms in the plutonic crust are able to survive within fractures or porous substrates by coupling sources of energy to organic and inorganic carbon resources that are probably delivered through the circulation of subseafloor fluids or seawater. 

Retracted: No

PubPeer comments:
 Authors and readers should become aware of a recent preprint deposited in bioRxiv entitled  Contesting the evidence for gene expression in lower oceanic crust From the abstract:  Li et al [Nature 579, 250u2013255 (2020)] report microbial gene expression in deep ocean crust, from microbial communities that have concentrations as low as 100 cell per cubic cm. This would be incredible, since that would be the lowest biomass sample ever analyzed for gene expression for a deep biosphere sample by several orders of magnitude. **However, I have reanalyzed the data and show that the authoru2019s data are derived from contamination via seawater, humans, human skin associated bacteria, drilling fluid, and molecular reagent kits. The method that the authors used to produce their gene expression data is highly sensitive to DNA contamination, which is the case here.** The authors claim that Pseudomonas, a known widespread contaminant in molecular reagent kits, is one of the most active groups in their lower crust samples and base their metabolic analysis on this contaminating organism. **Here, I show that the gene expression data are derived from contaminating Pseudomonas (as well as other groups), and I show that the groups claimed as being active in the rock samples are also present in the negative controls at similar or higher relative abundance.** For example, methane production in long term incubations was reported but gene expression from methanogens was 10 times higher in the drill fluid negative controls compared to the rock samples, demonstrating that the methane measured is likely derived from methanogen contaminants introduced from the drill fluid. There are no signs of active life here, but lipid biomarkers were found preserved in the rocks. Thus, the authors have sampled a fossilized biosphere, not a living one. ,