Smith David C.
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ArticleBacterial diversity and community composition from seasurface to subseafloor(Nature Publishing Group, 2015-10-02) Walsh, Emily A. ; Kirkpatrick, John B. ; Rutherford, Scott D. ; Smith, David C. ; Sogin, Mitchell L. ; D'Hondt, StevenWe investigated compositional relationships between bacterial communities in the water column and those in deep-sea sediment at three environmentally distinct Pacific sites (two in the Equatorial Pacific and one in the North Pacific Gyre). Through pyrosequencing of the v4–v6 hypervariable regions of the 16S ribosomal RNA gene, we characterized 450 104 pyrotags representing 29 814 operational taxonomic units (OTUs, 97% similarity). Hierarchical clustering and non-metric multidimensional scaling partition the samples into four broad groups, regardless of geographic location: a photic-zone community, a subphotic community, a shallow sedimentary community and a subseafloor sedimentary community (greater than or equal to1.5 meters below seafloor). Abundance-weighted community compositions of water-column samples exhibit a similar trend with depth at all sites, with successive epipelagic, mesopelagic, bathypelagic and abyssopelagic communities. Taxonomic richness is generally highest in the water-column O2 minimum zone and lowest in the subseafloor sediment. OTUs represented by abundant tags in the subseafloor sediment are often present but represented by few tags in the water column, and represented by moderately abundant tags in the shallow sediment. In contrast, OTUs represented by abundant tags in the water are generally absent from the subseafloor sediment. These results are consistent with (i) dispersal of marine sedimentary bacteria via the ocean, and (ii) selection of the subseafloor sedimentary community from within the community present in shallow sediment.
ArticleThe contribution of water radiolysis to marine sedimentary life(Nature Research, 2021-02-26) Sauvage, Justine ; Flinders, Ashton F. ; Spivack, Arthur J. ; Pockalny, Robert ; Dunlea, Ann G. ; Anderson, Chloe H. ; Smith, David C. ; Murray, Richard W. ; D'Hondt, StevenWater radiolysis continuously produces H2 and oxidized chemicals in wet sediment and rock. Radiolytic H2 has been identified as the primary electron donor (food) for microorganisms in continental aquifers kilometers below Earth’s surface. Radiolytic products may also be significant for sustaining life in subseafloor sediment and subsurface environments of other planets. However, the extent to which most subsurface ecosystems rely on radiolytic products has been poorly constrained, due to incomplete understanding of radiolytic chemical yields in natural environments. Here we show that all common marine sediment types catalyse radiolytic H2 production, amplifying yields by up to 27X relative to pure water. In electron equivalents, the global rate of radiolytic H2 production in marine sediment appears to be 1-2% of the global organic flux to the seafloor. However, most organic matter is consumed at or near the seafloor, whereas radiolytic H2 is produced at all sediment depths. Comparison of radiolytic H2 consumption rates to organic oxidation rates suggests that water radiolysis is the principal source of biologically accessible energy for microbial communities in marine sediment older than a few million years. Where water permeates similarly catalytic material on other worlds, life may also be sustained by water radiolysis.
ArticleAtribacteria reproducing over millions of years in the Atlantic abyssal subseafloor(American Society for Microbiology, 2020-10-06) Vuillemin, Aurèle ; Vargas, Sergio ; Coskun, Ömer K. ; Pockalny, Robert ; Murray, Richard W. ; Smith, David C. ; D'Hondt, Steven ; Orsi, William D.How microbial metabolism is translated into cellular reproduction under energy-limited settings below the seafloor over long timescales is poorly understood. Here, we show that microbial abundance increases an order of magnitude over a 5 million-year-long sequence in anoxic subseafloor clay of the abyssal North Atlantic Ocean. This increase in biomass correlated with an increased number of transcribed protein-encoding genes that included those involved in cytokinesis, demonstrating that active microbial reproduction outpaces cell death in these ancient sediments. Metagenomes, metatranscriptomes, and 16S rRNA gene sequencing all show that the actively reproducing community was dominated by the candidate phylum “Candidatus Atribacteria,” which exhibited patterns of gene expression consistent with fermentative, and potentially acetogenic, metabolism. “Ca. Atribacteria” dominated throughout the 8 million-year-old cored sequence, despite the detection limit for gene expression being reached in 5 million-year-old sediments. The subseafloor reproducing “Ca. Atribacteria” also expressed genes encoding a bacterial microcompartment that has potential to assist in secondary fermentation by recycling aldehydes and, thereby, harness additional power to reduce ferredoxin and NAD+. Expression of genes encoding the Rnf complex for generation of chemiosmotic ATP synthesis were also detected from the subseafloor “Ca. Atribacteria,” as well as the Wood-Ljungdahl pathway that could potentially have an anabolic or catabolic function. The correlation of this metabolism with cytokinesis gene expression and a net increase in biomass over the million-year-old sampled interval indicates that the “Ca. Atribacteria” can perform the necessary catabolic and anabolic functions necessary for cellular reproduction, even under energy limitation in millions-of-years-old anoxic sediments.
ArticleArchaea dominate oxic subseafloor communities over multimillion-year time scales(American Association for the Advancement of Science, 2019-06-19) Vuillemin, Aurèle ; Wankel, Scott D. ; Coskun, Ömer K. ; Magritsch, Tobias ; Vargas, Sergio ; Estes, Emily R. ; Spivack, Arthur J. ; Smith, David C. ; Pockalny, Robert ; Murray, Richard W. ; D'Hondt, Steven ; Orsi, William D.Ammonia-oxidizing archaea (AOA) dominate microbial communities throughout oxic subseafloor sediment deposited over millions of years in the North Atlantic Ocean. Rates of nitrification correlated with the abundance of these dominant AOA populations, whose metabolism is characterized by ammonia oxidation, mixotrophic utilization of organic nitrogen, deamination, and the energetically efficient chemolithoautotrophic hydroxypropionate/hydroxybutyrate carbon fixation cycle. These AOA thus have the potential to couple mixotrophic and chemolithoautotrophic metabolism via mixotrophic deamination of organic nitrogen, followed by oxidation of the regenerated ammonia for additional energy to fuel carbon fixation. This metabolic feature likely reduces energy loss and improves AOA fitness under energy-starved, oxic conditions, thereby allowing them to outcompete other taxa for millions of years.