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Different intensities of high temperatures affect the growth of photosynthetic cells in nature. To elucidate the underlying mechanisms, we cultivated the unicellular green alga Chlamydomonas reinhardtii under highly controlled photobioreactor conditions and revealed systems-wide shared and unique responses to 24-hour moderate (35°C) and acute (40°C) high temperatures and subsequent recovery at 25°C. We identified previously overlooked unique elements in response to moderate high temperature. Heat at 35°C transiently arrested the cell cycle followed by partial synchronization, up-regulated transcripts/proteins involved in gluconeogenesis/glyoxylate-cycle for carbon uptake, promoted growth, and increased starch accumulation. Heat at 40°C arrested the cell cycle, inhibited growth, resulting in carbon uptake over usage and increased starch accumulation. Both high temperatures induced photoprotection, while 40°C decreased photosynthetic efficiency, distorted thylakoid/pyrenoid ultrastructure, and affected the carbon concentrating mechanism. We demonstrated increased transcript/protein correlation during both heat treatments, suggesting reduced post-transcriptional regulation during heat may help coordinate heat tolerance activities efficiently. During recovery after both heat treatments, transcripts/proteins related to DNA synthesis increased while those involved in photosynthetic light reactions decreased. We propose down-regulating photosynthetic light reactions during DNA replication benefits cell cycle resumption by reducing ROS production. Our results provide potential targets to increase thermotolerance in algae and crops.