Variations in H2 thresholds and growth yields among hydrogenotrophic methanogens relate to different energy conservation strategies

Abstract

Hydrogenotrophic methanogens are of high environmental and biotechnological importance, converting CO2 with H2 into CH4. Despite their common metabolism, variations in the energy metabolism among these methanogens exist, likely affecting their H2 thresholds and growth yields. However, a systematic comparison of these traits for a wide range of hydrogenotrophic methanogens has been lacking. Here, we measured the H2 thresholds and growth yields of nine different hydrogenotrophic methanogens. The H2 threshold, i.e. the H2 partial pressure at which H2 consumption halts, ranged over two orders of magnitude from 1.0 {+/-} 0.5 Pa for Methanobrevibacter arboriphilus to 120 {+/-} 10 Pa for Methanosarcina mazei. Growth yields in our experimental conditions ranged from 0.51 {+/-} 0.28 gDCWx(mol CH4)-1 for Methanococcus maripaludis to 5.28 {+/-} 1.25 gDCWx(mol CH4)-1 for Methanosarcina mazei. The ATP gains, estimated from both H2 thresholds and growth yields, correlated reasonably well, confirming that these variations are due to differences in energy conservation strategies. Our results strongly differentiated the two previously proposed groups of hydrogenotrophic methanogens: methanogens with cytochromes had a high H2 threshold ([&ge;] 21 Pa) and high growth yield (> 4.0 gDCWx(mol CH4)-1), whereas methanogens without cytochromes had lower H2 threshold ([&le;] 7 Pa) and low growth yield (< 1.7 gDCWx(mol CH4)-1). Moreover, our H2 thresholds indicated that additional variations in energy metabolism exist within both groups. Overall, this study found strong variations between hydrogenotrophic methanogens, which are important to understand their environmental prevalence and biotechnological applicability. ImportanceHydrogenotrophic methanogens play key roles in natural ecosystems and biotechnological processes. Even though all hydrogenotrophic methanogens convert CO2 with H2 into CH4, they can differ in their H2 threshold and growth yield, due to variations in their energy metabolism. Here, we found that H2 thresholds of hydrogenotrophic methanogens range over two orders of magnitude, while a ten-fold difference was observed in their growth yields. These strong variations in H2 thresholds and growth yields demonstrate that hydrogenotrophic methanogens are confronted with a trade-off between the capacity to grow at low H2 levels (low H2 threshold) and efficient growth (high growth yield). Curiously, the observed H2 thresholds also correlate with the electroactivity of different hydrogenotrophic methanogens. Overall, by reporting H2 thresholds and growth yields for a wide range of hydrogenotrophic methanogens, this work provides new insights into the bioenergetic diversity of these microbes, as well as their environmental prevalence and biotechnological applicability.