Physiological adaptations to serpentinization in the Samail Ophiolite, Oman

Our plain-English summary of Physiological adaptations to serpentinization in the Samail Ophiolite, Oman, by E.M. Fones, D.R. Colman, E.A. Kraus, et al (The ISME Journal, 2019).

The study

• Authors: E.M. Fones, D.R. Colman, E.A. Kraus, D.B. Nothaft, S. Poudel, K.R. Rempfert, J.R. Spear, A.S. Templeton, E.S. Boyd
• Journal: The ISME Journal
• Published: 2019;13(7):1750-1762
• Cited by: 42 articles, as counted by NIH iCite
• Read it: PubMed · Publisher · Free full text

Abstract

Hydration of ultramafic rock during the geologic process of serpentinization can generate reduced substrates that microorganisms may use to fuel their carbon and energy metabolisms. However, serpentinizing environments also place multiple constraints on microbial life by generating highly reduced hyperalkaline waters that are limited in dissolved inorganic carbon. To better understand how microbial life persists under these conditions, we performed geochemical measurements on waters from a serpentinizing environment and subjected planktonic microbial cells to metagenomic and physiological analyses. Metabolic potential inferred from metagenomes correlated with fluid type, and genes involved in anaerobic metabolisms were enriched in hyperalkaline waters. The abundance of planktonic cells and their rates of utilization of select single-carbon compounds were lower in hyperalkaline waters than alkaline waters. However, the ratios of substrate assimilation to dissimilation were higher in hyperalkaline waters than alkaline waters, which may represent adaptation to minimize energetic and physiologic stress imposed by highly reducing, carbon-limited conditions. Consistent with this hypothesis, estimated genome sizes and average oxidation states of carbon in inferred proteomes were lower in hyperalkaline waters than in alkaline waters. These data suggest that microorganisms inhabiting serpentinized waters exhibit a unique suite of physiological adaptations that allow for their persistence under these polyextremophilic conditions.

In plain English

This study is about microbes in underground water in Oman's Samail Ophiolite, a rock formation. It does not study asbestos or human health. In February 2017 the authors sampled seven existing wells, one at two depths, giving eight samples. Water pH ranged from 7.6 to 11.3; the authors used pH as a rough guide to how far a rock-water reaction called serpentinization had progressed. They measured water chemistry and sequenced microbial DNA; for five wells they also counted cells and measured maximum potential carbon-use rates in laboratory bottles. Cell counts were lower in hyperalkaline (most alkaline) waters than in alkaline waters. Genes for oxygen-free living were more common in hyperalkaline waters. In these tests, higher pH went with lower potential rates of carbon monoxide use for energy and higher potential rates of formate built into cells. Average estimated genome size per sample ranged from 4.0 to 2.1 million base pairs, smaller at higher pH. The authors concluded that the findings suggest the microbes have adapted to these conditions. They noted they did not track some products, such as acetate.

We wrote this plain-English summary from the full article with the help of AI, and a second AI model checked each sentence against the article. It is not the authors' wording; the abstract and the article are their own account.

What the study did and found

• Design: Field study of groundwater microbial communities combining geochemical measurements, cell counts, metagenomic (community DNA) sequencing and laboratory microcosm assays with radiolabeled carbon compounds, which measured maximum potential transformation rates
• Who was studied: Microbial communities in water from seven previously drilled wells in the Samail Ophiolite, Sultanate of Oman, sampled in February 2017. One well (NSHQ14) was sampled at two depths (50 m and 85 m), giving eight samples. Water pH ranged from 7.6 to 11.3. Cell counts and microcosm rate assays used five of the wells.
• Exposure: No asbestos or fiber exposure was studied. The study compared water types (contact, alkaline peridotite, hyperalkaline peridotite) along a pH gradient, which the authors used as a proxy for serpentinization reaction progress.
• Main results:
  • Average cell concentrations were 3.77 × 10^5 cells per mL (WAB105) and 4.03 × 10^5 cells per mL (WAB104) in alkaline peridotite wells. They were 2.58 × 10^5 cells per mL (WAB71) and 1.16 × 10^5 cells per mL (NSHQ14) in hyperalkaline peridotite wells. The highest concentration, 7.28 × 10^5 cells per mL, was in the contact well WAB55.
  • Metagenomes from hyperalkaline peridotite wells were enriched in genes typically involved in anaerobic metabolism, including nickel-dependent CODH subunits.
  • In laboratory microcosms, maximum potential rates of carbon monoxide oxidation to carbon dioxide showed a significant inverse correlation with well-water pH (Pearson R = −0.94, p less than 0.05). For bicarbonate reduction to methane and formate oxidation to carbon dioxide, the negative correlations with pH were not statistically significant.
  • In the same microcosm assays, the potential rate of formate assimilation to biomass correlated positively with pH (Pearson R = 0.90, p less than 0.05).
  • In the microcosms, ratios of dissimilation to assimilation decreased in communities from higher-pH waters, for bicarbonate (Pearson R = 0.87) and for formate (Pearson R = 0.84), as printed. No relationship with pH was observed for carbon monoxide.
  • The mean estimated size of metagenome-assembled genomes per sample ranged from 4.0 Mbp (WAB105) to 2.1 Mbp (NSHQ14C) and showed a significant inverse correlation with pH (Pearson R = −0.82, p less than 0.05).
  • The average oxidation state of carbon in inferred proteins ranged from −0.01 (WAB104) to −0.28 (NSHQ14C) and correlated inversely with pH (Pearson R = −0.72, p less than 0.05).
• The authors' conclusion: The authors concluded that the observations suggest physiological adaptations that minimize energetic and physiological stress under the highly reducing, carbon-limited conditions of serpentinizing environments. In their view these adaptations include gene enrichment, greater carbon assimilation, smaller genomes and more reduced protein carbon.
• Limitations the authors state:
  • Production of radiolabeled acetate was not tracked in the microcosm assays, so the low dissimilation-to-assimilation ratios might reflect acetate production.
  • Methane production from radiolabeled formate or carbon monoxide was not tracked.
  • The failure to detect the methanogenesis gene mcrA in two wells may reflect undersampling of rare organisms.
  • Some field measurements reported for 2017 samples were taken from 2016 (or 2015) data because they were not collected in 2017.

Topics

The National Library of Medicine indexes this study under subjects our site covers: Chrysotile.

Medical terms in this study, explained in our Lexicon: Serpentinization, Ophiolite, Ultramafic Rocks.

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