Biomethanation is a crucial process occurring in natural and engineered systems which can reduce carbon dioxide to methane impacting the global carbon cycle. However, little is known about the effect of on-and-off gaseous provision and micronutrients on bioconversion. Here, anaerobic microbiomes underwent intermittent feeding with incremental starvations and selective metal supplementation to assess the impact of hydrogen and carbon dioxide availability on microbial physiology. Resilience was tested under differential cultivations in basal medium supplemented with either nickel or cobalt. Nickel-augmented cultures exhibited faster recovery upon starvation, suggesting a beneficial effect. Dominant Methanothermobacter thermautotrophicus demonstrated robust growth, genetic stability and transcriptional downregulation when starved. Conversely, bacteria were plastic and prone to genetic fluctuations, accumulating mutations on genes encoding for ABC-transporters and C-metabolism enzymes. This study pioneers cellular resilience and response to micronutrient supplementation in anaerobic carbon dioxide-fixating microbiomes, offering valuable insights into microbial activity recovery after carbon and electron donor deprivation.