The Chlamydomonas reinhardtii chloroplast envelope protein LCIA transports bicarbonate in planta

LCIA (low CO2-inducible protein A) is a chloroplast envelope protein associated with the CO2-concentrating mechanism of the green alga Chlamydomonas reinhardtii. LCIA is postulated to be a HCO3- channel, but previous studies were unable to show that LCIA was actively transporting bicarbonate in plan...

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Published in:	Journal of experimental botany Vol. 74; no. 12; pp. 3651 - 3666
Main Authors:	Förster, Britta, Rourke, Loraine M, Weerasooriya, Hiruni N, Pabuayon, Isaiah C M, Rolland, Vivien, Au, Eng Kee, Bala, Soumi, Bajsa-Hirschel, Joanna, Kaines, Sarah, Kasili, Remmy W, LaPlace, Lillian M, Machingura, Marylou C, Massey, Baxter, Rosati, Viviana C, Stuart-Williams, Hilary, Badger, Murray R, Price, G Dean, Moroney, James V
Format:	Journal Article
Language:	English
Published:	England 27-06-2023
Subjects:	Bicarbonates - metabolism Carbon Dioxide - metabolism Carbonic Anhydrases - genetics Carbonic Anhydrases - metabolism Chlamydomonas reinhardtii - genetics Chlamydomonas reinhardtii - metabolism Chloroplasts - metabolism Photosynthesis Plants - metabolism Bicarbonate transport photosynthesis carbonic anhydrase βca5 DCAKO CCM LCIA
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Abstract	LCIA (low CO2-inducible protein A) is a chloroplast envelope protein associated with the CO2-concentrating mechanism of the green alga Chlamydomonas reinhardtii. LCIA is postulated to be a HCO3- channel, but previous studies were unable to show that LCIA was actively transporting bicarbonate in planta. Therefore, LCIA activity was investigated more directly in two heterologous systems: an Escherichia coli mutant (DCAKO) lacking both native carbonic anhydrases and an Arabidopsis mutant (βca5) missing the plastid carbonic anhydrase βCA5. Neither DCAKO nor βca5 can grow in ambient CO2 conditions, as they lack carbonic anhydrase-catalyzed production of the necessary HCO3- concentration for lipid and nucleic acid biosynthesis. Expression of LCIA restored growth in both systems in ambient CO2 conditions, which strongly suggests that LCIA is facilitating HCO3- uptake in each system. To our knowledge, this is the first direct evidence that LCIA moves HCO3- across membranes in bacteria and plants. Furthermore, the βca5 plant bioassay used in this study is the first system for testing HCO3- transport activity in planta, an experimental breakthrough that will be valuable for future studies aimed at improving the photosynthetic efficiency of crop plants using components from algal CO2-concentrating mechanisms.
AbstractList	LCIA (low CO2-inducible protein A) is a chloroplast envelope protein associated with the CO2-concentrating mechanism of the green alga Chlamydomonas reinhardtii. LCIA is postulated to be a HCO3- channel, but previous studies were unable to show that LCIA was actively transporting bicarbonate in planta. Therefore, LCIA activity was investigated more directly in two heterologous systems: an Escherichia coli mutant (DCAKO) lacking both native carbonic anhydrases and an Arabidopsis mutant (βca5) missing the plastid carbonic anhydrase βCA5. Neither DCAKO nor βca5 can grow in ambient CO2 conditions, as they lack carbonic anhydrase-catalyzed production of the necessary HCO3- concentration for lipid and nucleic acid biosynthesis. Expression of LCIA restored growth in both systems in ambient CO2 conditions, which strongly suggests that LCIA is facilitating HCO3- uptake in each system. To our knowledge, this is the first direct evidence that LCIA moves HCO3- across membranes in bacteria and plants. Furthermore, the βca5 plant bioassay used in this study is the first system for testing HCO3- transport activity in planta, an experimental breakthrough that will be valuable for future studies aimed at improving the photosynthetic efficiency of crop plants using components from algal CO2-concentrating mechanisms.
Author	Bala, Soumi Massey, Baxter Moroney, James V Machingura, Marylou C Förster, Britta LaPlace, Lillian M Au, Eng Kee Rolland, Vivien Kaines, Sarah Price, G Dean Badger, Murray R Pabuayon, Isaiah C M Weerasooriya, Hiruni N Rourke, Loraine M Rosati, Viviana C Bajsa-Hirschel, Joanna Kasili, Remmy W Stuart-Williams, Hilary
Author_xml	– sequence: 1 givenname: Britta orcidid: 0000-0002-5231-0954 surname: Förster fullname: Förster, Britta organization: The Australian National University, Canberra, ACT 2600, Australia – sequence: 2 givenname: Loraine M orcidid: 0000-0002-2600-8073 surname: Rourke fullname: Rourke, Loraine M organization: The Australian National University, Canberra, ACT 2600, Australia – sequence: 3 givenname: Hiruni N orcidid: 0000-0001-8163-8126 surname: Weerasooriya fullname: Weerasooriya, Hiruni N organization: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA – sequence: 4 givenname: Isaiah C M surname: Pabuayon fullname: Pabuayon, Isaiah C M organization: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA – sequence: 5 givenname: Vivien orcidid: 0000-0002-9232-1287 surname: Rolland fullname: Rolland, Vivien organization: CSIRO Agriculture and Food, Canberra, ACT 2601, Australia – sequence: 6 givenname: Eng Kee surname: Au fullname: Au, Eng Kee organization: The Australian National University, Canberra, ACT 2600, Australia – sequence: 7 givenname: Soumi surname: Bala fullname: Bala, Soumi organization: The Australian National University, Canberra, ACT 2600, Australia – sequence: 8 givenname: Joanna orcidid: 0000-0001-7607-5808 surname: Bajsa-Hirschel fullname: Bajsa-Hirschel, Joanna organization: Natural Products Utilization Research Unit, United States Department of Agriculture, University, MS 38677, USA – sequence: 9 givenname: Sarah surname: Kaines fullname: Kaines, Sarah organization: The Australian National University, Canberra, ACT 2600, Australia – sequence: 10 givenname: Remmy W orcidid: 0000-0002-0525-4515 surname: Kasili fullname: Kasili, Remmy W organization: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA – sequence: 11 givenname: Lillian M orcidid: 0000-0002-0245-5952 surname: LaPlace fullname: LaPlace, Lillian M organization: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA – sequence: 12 givenname: Marylou C orcidid: 0000-0002-7932-4192 surname: Machingura fullname: Machingura, Marylou C organization: Biology Department, Georgia Southern University, Savannah, GA 31419, USA – sequence: 13 givenname: Baxter orcidid: 0000-0001-8435-3791 surname: Massey fullname: Massey, Baxter organization: The Australian National University, Canberra, ACT 2600, Australia – sequence: 14 givenname: Viviana C orcidid: 0000-0003-1947-0689 surname: Rosati fullname: Rosati, Viviana C organization: Department of Biology, Centre for Novel Agricultural Products (CNAP), University of York, Wentworth Way, York YO10 5DD, UK – sequence: 15 givenname: Hilary orcidid: 0000-0002-9272-9178 surname: Stuart-Williams fullname: Stuart-Williams, Hilary organization: The Australian National University, Canberra, ACT 2600, Australia – sequence: 16 givenname: Murray R orcidid: 0000-0001-9428-2579 surname: Badger fullname: Badger, Murray R organization: The Australian National University, Canberra, ACT 2600, Australia – sequence: 17 givenname: G Dean orcidid: 0000-0001-5906-4912 surname: Price fullname: Price, G Dean organization: The Australian National University, Canberra, ACT 2600, Australia – sequence: 18 givenname: James V orcidid: 0000-0002-3652-5293 surname: Moroney fullname: Moroney, James V organization: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA
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Copyright	The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.
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Keywords	Bicarbonate transport photosynthesis carbonic anhydrase βca5 DCAKO CCM LCIA
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Snippet	LCIA (low CO2-inducible protein A) is a chloroplast envelope protein associated with the CO2-concentrating mechanism of the green alga Chlamydomonas...
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SubjectTerms	Bicarbonates - metabolism Carbon Dioxide - metabolism Carbonic Anhydrases - genetics Carbonic Anhydrases - metabolism Chlamydomonas reinhardtii - genetics Chlamydomonas reinhardtii - metabolism Chloroplasts - metabolism Photosynthesis Plants - metabolism
Title	The Chlamydomonas reinhardtii chloroplast envelope protein LCIA transports bicarbonate in planta
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