<p><i>Chlamydomonas reinhardtii</i> as a mixotroph is able to use both autotrophic and heterotrophic sources of energy and carbon. But, the importance of sources of energy and carbon varies among mixotrophs and circumstances. This study evaluates the importance of autotrophic and heterotrophic inputs, and analyzes metabolic flexibility in the context of managing the cell's carbon and energy budgets. Examining wild type and mutants with defects in photosynthesis, respiration, and acetate assimilation revealed that growth of mixotrophic cells relies on photosynthesis as a primary source of energy and acetate as a major source of carbon. To shed light on how autotrophic and heterotrophic inputs influence central metabolism, metabolite profiling and gene expression analysis were studied. The tricarboxylic acid cycle was found as a central hub for compensatory adjustments, with variations in metabolite accumulation and gene expression reflecting altered activity. Changes in the redistribution of energy between plastid and cytosol through malate valves, triose phosphate shuttles and ATP transporters were supposed to be another part of the mechanism that ensured the optimization of metabolism at different trophic states. Upregulation of the glyoxylate pathway could fully compensate for the deficiency in carbon fixation caused by the lack of Rubisco activase. Thus, metabolic rearrangement cannot compensate for the lack of ability to incorporate carbon from acetate. In turn, activation of the tricarboxylic cycle is unable to reimburse impaired photosynthetic energy production. Therefore, rearrangements of energy generation and redistribution compensate for mitochondrial respiration deficiency. Thus, microalgae cells demonstrated high but limited potential of metabolic adaptation to trophic constraints.</p>