Taxis toward hydrogen gas by Methanococcus maripaludis

Abstract

Knowledge of taxis (directed swimming) in the Archaea is currently expanding through identification of novel receptors, effectors, and proteins involved in signal transduction to the flagellar motor. Although the ability for biological cells to sense and swim toward hydrogen gas has been hypothesized for many years, this capacity has yet to be observed and demonstrated. Here we show that the average swimming velocity increases in the direction of a source of hydrogen gas for the methanogen, Methanococcus maripaludis using a capillary assay with anoxic gas-phase control and time-lapse microscopy. The results indicate that a methanogen couples motility to hydrogen concentration sensing and is the first direct observation of hydrogenotaxis in any domain of life. Hydrogenotaxis represents a strategy that would impart a competitive advantage to motile microorganisms that compete for hydrogen gas and would impact the C, S and N cycles.

Figure 1. The predicted hydrogen concentration over time at the observation point 0.5 cm from the gas phase over the course of the experiment shown with (A) linear axes and (B) log-linear axes.

The 2.5–23 μM threshold, at which hydrogenotrophic methanogens have been shown to use H₂ in pure culture studies, is reached at approximately 10 minutes.

Figure 2. Average cell velocity (black) with 95% confidence intervals (gray) before and after opening valve to gas phase for (A) H₂ and (B) Ar control.

Positive y-axis values indicate movement toward the gas phase, negative y-axis values indicate movement away from the gas phase. Average cell velocity (C) and (D) normal to concentration gradient (n = 5 for H₂ and n = 3 for Ar).

Figure 3. Swimming speed of M. maripaludis cells when starved for 5 hours before H₂ exposure (−H₂ and n = 4,725), after H₂ exposure (+H₂ and n = 20,189), and when not starved (No starve, n = 45,001).

Values represent the mean and error bars represent 95% confidence intervals. (A) Average swimming speed. The difference between –H₂ and both +H₂ and no starvation is significant (p < 0.05). (B) Average maximum swimming speeds are represented by bars, and absolute maximum values inside each bar represent the highest observed speed over all time points for the condition. Differences between all conditions are significant (p < 0.05) and p values were calculated with two-tailed t-tests.

Figure 4. Model fitting results (smooth black lines) overlaid on experimental results with 95% confidence intervals (grey lines) (A) using average literature values for χ and μ and varying k_d over the range shown or (B) using average literature values for k_d and μ while varying χ over the range shown (C) or μ varied across the range of literature values.

Figure 5. (A) and (B) Field emission scanning electron micrographs of M. maripaludis pellicle with extracellular material and cells (indicated by arrows in (A)).