Abstract
Thermodynamic models predict that H2 is energetically favorable for seafloor microbial life, but how H2 affects anabolic processes in seafloor-associated communities is poorly understood. Here, we used quantitative 13C DNA stable isotope probing (qSIP) to quantify the effect of H2 on carbon assimilation by microbial taxa synthesizing 13C-labeled DNA that are associated with partially serpentinized peridotite rocks from the equatorial Mid-Atlantic Ridge. The rock-hosted seafloor community was an order of magnitude more diverse compared to the seawater community directly above the rocks. With added H2, peridotite-associated taxa increased assimilation of 13C-bicarbonate and 13C-acetate into 16S rRNA genes of operational taxonomic units by 146% (±29%) and 55% (±34%), respectively, which correlated with enrichment of H2-oxidizing NiFe-hydrogenases encoded in peridotite-associated metagenomes. The effect of H2 on anabolism was phylogenetically organized, with taxa affiliated with Atribacteria, Nitrospira, and Thaumarchaeota exhibiting the most significant increases in 13C-substrate assimilation in the presence of H2. In SIP incubations with added H2, an order of magnitude higher number of peridotite rock-associated taxa assimilated 13C-bicarbonate, 13C-acetate, and 13C-formate compared to taxa that were not associated with peridotites. Collectively, these findings indicate that the unique geochemical nature of the peridotite-hosted ecosystem has selected for H2-metabolizing, rock-associated taxa that can increase anabolism under high H2 concentrations. Because ultramafic rocks are widespread in slow-, and ultraslow-spreading oceanic lithosphere, continental margins, and subduction zones where H2 is formed in copious amounts, the link between H2 and carbon assimilation demonstrated here may be widespread within these geological settings.
Highlights
The oxidation of molecular hydrogen (H2) is an important source of bioavailable energy in anoxic environments, and H2 represents a key metabolic intermediate in anaerobic syntrophy [1, 2].Recently, aerobic H2 oxidation was discovered to be widespread amongst microbial “dark matter” [3,4,5], with many aerobic microbial groups being capable of scavenging trace concentrations of atmospheric H2 as an energy source [6]
Microbial abundance and diversity of the ultramafic-rock associated community The concentration of 16S ribosomal RNA (rRNA) genes from the peridotite rock samples was 2.6 (±2)×104 copies per g of rock, compared to 7 (±1)×104 and 0.5 (±0.06)×104 16S rRNA gene copies per mL seawater collected with the isobaric gas-tight (IGT) fluid samplers and Niskin rosette, respectively (Fig. 2B). Quantitative PCR (qPCR) quantification of 16S rRNA gene copies from the frozen peridotite rock samples showed cycle threshold (Ct) values ranging between 25 and 30 cycles, which strongly indicates that our amplified 16S rRNA genes are derived from in situ microbes associated with the rocks as opposed to contamination because all contamination controls consistently had Ct values >35
The Chao diversity index based on the 16S rRNA gene data shows that the rock-associated community is significantly more diverse compared to the seawater communities (Fig. 3B). 16S rRNA gene data shows that the microbial community composition between the peridotite-associated and the seawater communities was significantly different (Analysis of Similarity [ANOSIM] R: 0.87, P < 0.0001), with approximately two-thirds of all detected operational taxonomic units (OTUs) being found on the peridotite rock samples and not in any seawater samples (Fig. 3C)
Summary
The oxidation of molecular hydrogen (H2) is an important source of bioavailable energy in anoxic environments, and H2 represents a key metabolic intermediate in anaerobic syntrophy [1, 2].Recently, aerobic H2 oxidation was discovered to be widespread amongst microbial “dark matter” [3,4,5], with many aerobic microbial groups being capable of scavenging trace concentrations of atmospheric H2 as an energy source [6]. To better understand the effects of H2 on carbon anabolism in seafloor microbial communities associated with ultramafic rocks, we used 13C quantitative DNA stable isotope probing (qSIP) [13, 14] with 13C-labeled bicarbonate, acetate, and formate in H2 incubation experiments. The 13C DNA-qSIP approach identifies microbial taxa that are synthesizing new 13C-labeled DNA from the added 13C substrates, which occurs during genome replication [15]. We applied this method to microbial communities associated with partially serpentinized peridotite mylonite from Saint Peter and Saint Paul Archipelago (Arquipélago de São Pedro e São Paulo, Brasil ‘SPSPA’) at the equatorial Mid-Atlantic Ridge
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