Biological methane utilization, one of the main sinks of the greenhouse gas in nature, represents an attractive platform for production of fuels and value-added chemicals. Despite the progress made in our understanding of the individual parts of methane utilization, our knowledge of how the whole-cell metabolic network is organized and coordinated is limited. Attractive growth and methane-conversion rates, a complete and expert-annotated genome sequence, as well as large enzymatic, <
sup>
13<
/sup>
C-labeling, and transcriptomic datasets make <
i>
Methylomicrobium alcaliphilum<
/i>
20Z<
sup>
R<
/sup>
an exceptional model system for investigating methane utilization networks. Here we present a comprehensive metabolic framework of methane and methanol utilization in <
i>
M. alcaliphilum<
/i>
20Z<
sup>
R<
/sup>
. A set of novel metabolic reactions governing carbon distribution across central pathways in methanotrophic bacteria was predicted by in-silico simulations and confirmed by global non-targeted metabolomics and enzymatic evidences. Our data highlight the importance of substitution of ATP-linked steps with PPi-dependent reactions and support the presence of a carbon shunt from acetyl-CoA to the pentose-phosphate pathway and highly branched TCA cycle. The diverged TCA reactions promote balance between anabolic reactions and redox demands. As a result, the computational framework of C<
sub>
1<
/sub>
-metabolism in methanotrophic bacteria can represent an efficient tool for metabolic engineering or ecosystem modeling.