PMID- 35596080 OWN - NLM STAT- MEDLINE DCOM- 20220524 LR - 20220930 IS - 2055-0278 (Electronic) IS - 2055-0278 (Linking) VI - 8 IP - 5 DP - 2022 May TI - Modelling the pyrenoid-based CO(2)-concentrating mechanism provides insights into its operating principles and a roadmap for its engineering into crops. PG - 583-595 LID - 10.1038/s41477-022-01153-7 [doi] AB - Many eukaryotic photosynthetic organisms enhance their carbon uptake by supplying concentrated CO(2) to the CO(2)-fixing enzyme Rubisco in an organelle called the pyrenoid. Ongoing efforts seek to engineer this pyrenoid-based CO(2)-concentrating mechanism (PCCM) into crops to increase yields. Here we develop a computational model for a PCCM on the basis of the postulated mechanism in the green alga Chlamydomonas reinhardtii. Our model recapitulates all Chlamydomonas PCCM-deficient mutant phenotypes and yields general biophysical principles underlying the PCCM. We show that an effective and energetically efficient PCCM requires a physical barrier to reduce pyrenoid CO(2) leakage, as well as proper enzyme localization to reduce futile cycling between CO(2) and HCO(3)(-). Importantly, our model demonstrates the feasibility of a purely passive CO(2) uptake strategy at air-level CO(2), while active HCO(3)(-) uptake proves advantageous at lower CO(2) levels. We propose a four-step engineering path to increase the rate of CO(2) fixation in the plant chloroplast up to threefold at a theoretical cost of only 1.3 ATP per CO(2) fixed, thereby offering a framework to guide the engineering of a PCCM into land plants. CI - (c) 2022. The Author(s). FAU - Fei, Chenyi AU - Fei C AUID- ORCID: 0000-0002-8287-4347 AD - Department of Molecular Biology, Princeton University, Princeton, NJ, USA. AD - Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ, USA. FAU - Wilson, Alexandra T AU - Wilson AT AUID- ORCID: 0000-0002-1676-000X AD - Department of Molecular Biology, Princeton University, Princeton, NJ, USA. AD - Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA. FAU - Mangan, Niall M AU - Mangan NM AUID- ORCID: 0000-0002-3491-8341 AD - Department of Engineering Sciences and Applied Mathematics, Northwestern University, Evanston, IL, USA. niall.mangan@northwestern.edu. FAU - Wingreen, Ned S AU - Wingreen NS AUID- ORCID: 0000-0001-7384-2821 AD - Department of Molecular Biology, Princeton University, Princeton, NJ, USA. wingreen@princeton.edu. AD - Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ, USA. wingreen@princeton.edu. FAU - Jonikas, Martin C AU - Jonikas MC AUID- ORCID: 0000-0002-9519-6055 AD - Department of Molecular Biology, Princeton University, Princeton, NJ, USA. mjonikas@princeton.edu. AD - Howard Hughes Medical Institute, Princeton University, Princeton, NJ, USA. mjonikas@princeton.edu. LA - eng GR - R01 GM140032/GM/NIGMS NIH HHS/United States GR - 55108535/HHMI/Howard Hughes Medical Institute/United States PT - Journal Article DEP - 20220519 PL - England TA - Nat Plants JT - Nature plants JID - 101651677 RN - 142M471B3J (Carbon Dioxide) RN - EC 4.1.1.39 (Ribulose-Bisphosphate Carboxylase) SB - IM MH - *Carbon Dioxide/metabolism MH - *Chlamydomonas reinhardtii/genetics/metabolism MH - Chloroplasts/metabolism MH - Crops, Agricultural/genetics/metabolism MH - Photosynthesis/genetics MH - Plastids/metabolism MH - Ribulose-Bisphosphate Carboxylase/genetics/metabolism PMC - PMC9122830 COIS- The authors declare no competing interests. EDAT- 2022/05/21 06:00 MHDA- 2022/05/25 06:00 PMCR- 2022/05/19 CRDT- 2022/05/20 23:33 PHST- 2021/08/04 00:00 [received] PHST- 2022/04/11 00:00 [accepted] PHST- 2022/05/20 23:33 [entrez] PHST- 2022/05/21 06:00 [pubmed] PHST- 2022/05/25 06:00 [medline] PHST- 2022/05/19 00:00 [pmc-release] AID - 10.1038/s41477-022-01153-7 [pii] AID - 1153 [pii] AID - 10.1038/s41477-022-01153-7 [doi] PST - ppublish SO - Nat Plants. 2022 May;8(5):583-595. doi: 10.1038/s41477-022-01153-7. Epub 2022 May 19.