Different intensities of high temperatures affect plant growth and yield in the field, but the underlying mechanisms remain elusive. Using the unicellular green alga, Chlamydomonas reinhardtii, under highly controlled photobioreactor conditions, we revealed systems-wide shared and unique responses to 24-hour moderate (35oC) and acute (40oC) high temperatures and subsequent recovery at 25oC. Heat at 35oC increased transcripts/proteins involved in gluconeogensis/glyoxylate-cycle for carbon uptake, promoted growth, and increased starch accumulation. Heat at 40oC inhibited growth, resulting in carbon uptake over usage and increased starch accumulation. Heat at 35oC transiently inhabited the cell cycle followed by partial synchronization while 40oC inhibited DNA replication and arrested cell cycle. Both high temperatures induced photoprotection, while 40oC decreased photosynthetic efficiencies, distorted thylakoid/pyrenoid ultrastructure, and affected carbon concentrating mechanism. We demonstrated increased transcript/protein correlation during heat, which decreased during recovery, suggesting reduced post-transcriptional regulation during heat may help coordinate heat tolerance activities efficiently. During recovery after both 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. Furthermore, we identified transcripts/proteins with unique differential regulation at 35oC, uncovering previously overlooked novel elements in response to moderate high temperature. Our research improves understanding of heat responses in photosynthetic cells and provides potential targets to increase thermotolerance in algae and crops.