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Bioinformatic analysis of the distribution of inorganic carbon transporters and prospective targets for bioengineering to increase Ci uptake by cyanobacteria

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Abstract

Cyanobacteria have evolved a carbon-concentrating mechanism (CCM) which has enabled them to inhabit diverse environments encompassing a range of inorganic carbon (Ci: \({\text{HCO}}_{3}^{ - }\) and CO2) concentrations. Several uptake systems facilitate inorganic carbon accumulation in the cell, which can in turn be fixed by ribulose 1,5-bisphosphate carboxylase/oxygenase. Here we survey the distribution of genes encoding known Ci uptake systems in cyanobacterial genomes and, using a pfam- and gene context-based approach, identify in the marine (alpha) cyanobacteria a heretofore unrecognized number of putative counterparts to the well-known Ci transporters of beta cyanobacteria. In addition, our analysis shows that there is a huge repertoire of transport systems in cyanobacteria of unknown function, many with homology to characterized Ci transporters. These can be viewed as prospective targets for conversion into ancillary Ci transporters through bioengineering. Increasing intracellular Ci concentration coupled with efforts to increase carbon fixation will be beneficial for the downstream conversion of fixed carbon into value-added products including biofuels. In addition to CCM transporter homologs, we also survey the occurrence of rhodopsin homologs in cyanobacteria, including bacteriorhodopsin, a class of retinal-binding, light-activated proton pumps. Because they are light driven and because of the apparent ease of altering their ion selectivity, we use this as an example of re-purposing an endogenous transporter for the augmentation of Ci uptake by cyanobacteria and potentially chloroplasts.

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References

  • Aravind L, Koonin EV (2000) The STAS domain—a link between anion transporters and antisigma-factor antagonists. Curr Biol 10(2):R53–R55

    Article  CAS  PubMed  Google Scholar 

  • Axen SD, Erbilgin O, Kerfeld CA (2014) A Taxonomy of bacterial microcompartment loci constructed by a novel scoring method. PLoS Comput Biol 10(10):e1003898

    Article  PubMed Central  PubMed  Google Scholar 

  • Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54(383):609–622

    Article  CAS  PubMed  Google Scholar 

  • Balashov SP, Imasheva ES, Boichenko VA, Anton J, Wang JM, Lanyi JK (2005) Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 309(5743):2061–2064

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Battchikova N, Eisenhut M, Aro AM (2011) Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles. Biochim Biophys Acta 18:935–944

    Article  Google Scholar 

  • Bogomolni RA, Spudich JL (1982) Identification of a third rhodopsin-like pigment in phototactic Halobacterium halobium. Proc Natl Acad Sci USA 79(20):6250–6254

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bonfil DJ, Ronen-Tarazi M, Sültemeyer D, Lieman-Hurwitz J, Schatz D, Kaplan A (1998) A putative HCO3 − transporter in the cyanobacterium Synechococcus sp. strain PCC 7942. FEBS Lett 430(3):236–240

    Article  CAS  PubMed  Google Scholar 

  • Dufresne A, Ostrowski M, Scanlan DJ, Garczarek L, Mazard S, Palenik BP, Paulsen IT, Tandeau de Marsac N, Wincker P, Dossat C, Ferriera S, Johnson J, Post AF, Hess WR, Partensky F (2008) Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria. Genome Biol 9(5):R90

    Article  PubMed Central  PubMed  Google Scholar 

  • Duschl A, Lanyi JK, Zimanyi L (1990) Properties and photochemistry of a halorhodopsin from the haloalkalophile, Natronobacterium pharaonis. J Biol Chem 265(3):1261–1267

    CAS  PubMed  Google Scholar 

  • Folea IM, Zhang P, Nowaczyk MM, Ogawa T, Aro E-M, Boekema EJ (2008) Single particle analysis of thylakoid proteins from Thermosynechococcus elongatus and Synechocystis 6803: localization of the CupA subunit of NDH-1. FEBS Lett 582(2):249–254

    Article  CAS  PubMed  Google Scholar 

  • Forchhammer K, Tandeau de Marsac N (1995) Functional analysis of the phosphoprotein PII (glnB gene product) in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 177(8):2033–2040

  • Fridlyand L, Kaplan A, Reinhold L (1996) Quantitative evaluation of the role of a putative CO2-scavenging entity in the cyanobacterial CO2-concentrating mechanism. BioSyst 37(3):229–238

    Article  CAS  Google Scholar 

  • Gaudana SB, Alagesan S, Chetty M, Wangikar PP (2013) Diurnal rhythm of a unicellular diazotrophic cyanobacterium under mixotrophic conditions and elevated carbon dioxide. Photosynth Res 118(1–2):51–57

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto K, Choi AR, Furutani Y, Jung KH, Kandori H (2010) Low-temperature FTIR study of Gloeobacter rhodopsin: presence of strongly hydrogen-bonded water and long-range structural protein perturbation upon retinal photoisomerization. Biochemistry 49(15):3343–3350

    Article  CAS  PubMed  Google Scholar 

  • Hess W, Rocap G, Ting C, Larimer F, Stilwagen S, Lamerdin J, Chisholm S (2001) The photosynthetic apparatus of Prochlorococcus: insights through comparative genomics. Photosynth Res 70(1):53–71

    Article  CAS  PubMed  Google Scholar 

  • Imasheva ES, Balashov SP, Choi AR, Jung KH, Lanyi JK (2009) Reconstitution of Gloeobacter violaceus rhodopsin with a light-harvesting carotenoid antenna. Biochemistry 48(46):10948–10955

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jung KH, Trivedi VD, Spudich JL (2003) Demonstration of a sensory rhodopsin in eubacteria. Mol Microbiol 47(6):1513–1522

    Article  CAS  PubMed  Google Scholar 

  • Kawanabe A, Furutani Y, Jung K-H, Kandori H (2011) An inward proton transport using Anabaena sensory rhodopsin. J Microbiol 49(1):1–6

    Article  CAS  PubMed  Google Scholar 

  • Kim SY, Yoon SR, Han S, Yun Y, Jung KH (2014) A role of Anabaena sensory rhodopsin transducer (ASRT) in photosensory transduction. Mol Microbiol 93(3):403–414

    Article  CAS  PubMed  Google Scholar 

  • Kinney JN, Salmeen A, Cai F, Kerfeld CA (2012) Elucidating essential role of conserved carboxysomal protein CcmN reveals common feature of bacterial microcompartment assembly. J Biol Chem 287(21):17729–17736

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Klughammer B, Sultemeyer D, Badger MR, Price GD (1999) The involvement of NAD(P)H dehydrogenase subunits, NdhD3 and NdhF3, in high-affinity CO2 uptake in Synechococcus sp. PCC7002 gives evidence for multiple NDH-1 complexes with specific roles in cyanobacteria. Mol Microbiol 32(6):1305–1315

    Article  CAS  PubMed  Google Scholar 

  • Koropatkin NM, Koppenaal DW, Pakrasi HB, Smith TJ (2007) The structure of a cyanobacterial bicarbonate transport protein, CmpA. J Biol Chem 282(4):2606–2614

    Article  CAS  PubMed  Google Scholar 

  • Lieman-Hurwitz J, Rachmilevitch S, Mittler R, Marcus Y, Kaplan A (2003) Enhanced photosynthesis and growth of transgenic plants that express ictB, a gene involved in HCO3 − accumulation in cyanobacteria. Plant Biotech J 1(1):43–50

    Article  CAS  Google Scholar 

  • Ludwig M, Bryant DA (2012) Synechococcus sp. strain PCC 7002 transcriptome: acclimation to temperature, salinity, oxidative stress, and mixotrophic growth conditions. Front Microbiol 3:354

    PubMed Central  CAS  PubMed  Google Scholar 

  • Maeda S, Omata T (1997) Substrate-binding lipoprotein of the cyanobacterium Synechococcus sp. strain PCC 7942 involved in the transport of nitrate and nitrite. J Biol Chem 272(5):3036–3041

    Article  CAS  PubMed  Google Scholar 

  • Maeda S, Price GD, Badger MR, Enomoto C, Omata T (2000) Bicarbonate binding activity of the CmpA protein of the cyanobacterium Synechococcus sp. strain PCC 7942 involved in active transport of bicarbonate. J Biol Chem 275(27):20551–20555

    Article  CAS  PubMed  Google Scholar 

  • Maeda S, Badger MR, Price GD (2002) Novel gene products associated with NdhD3/D4-containing NDH-1 complexes are involved in photosynthetic CO2 hydration in the cyanobacterium, Synechococcus sp. PCC7942. Mol Microbiol 43(2):425–435

    Article  CAS  PubMed  Google Scholar 

  • Miranda MR, Choi AR, Shi L, Bezerra AG Jr, Jung KH, Brown LS (2009) The photocycle and proton translocation pathway in a cyanobacterial ion-pumping rhodopsin. Biophys J 96(4):1471–1481

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oesterhelt D, Stoeckenius W (1971) Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nat New Biol 233(39):149–152

    Article  CAS  PubMed  Google Scholar 

  • Ogawa T (1991) A gene homologous to the subunit-2 gene of Nadh dehydrogenase is essential to inorganic carbon transport of Synechocystis Pcc 6803. Proc Natl Acad Sci USA 88(10):4275–4279

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ogawa T, Kaplan A (2003) Inorganic carbon acquisition systems in cyanobacteria. Photosynth Res 77(2–3):105–115

    Article  CAS  PubMed  Google Scholar 

  • Ogawa T, Mi H (2007) Cyanobacterial NADPH dehydrogenase complexes. Photosynth Res 93(1–3):69–77

    Article  CAS  PubMed  Google Scholar 

  • Ohkawa H, Price GD, Badger MR, Ogawa T (2000) Mutation of ndh genes leads to inhibition of CO2 uptake rather than HCO3 − uptake in Synechocystis sp. strain PCC 6803. J Bacteriol 182(9):2591–2596

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Omata T, Price GD, Badger, Okamura M, Gohta S, Ogawa T (1999) Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. Proc Natl Acad Sci USA 96(23):13571–13576

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Omata T, Gohta S, Takahashi Y, Harano Y, Maeda S (2001) Involvement of a CbbR homolog in low CO2-induced activation of the bicarbonate transporter operon in cyanobacteria. J Bacteriol 183(6):1891–1898

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Omata T, Takahashi Y, Yamaguchi O, Nishimura T (2002) Structure, function and regulation of the cyanobacterial high-affinity bicarbonate transporter, BCT1. Funct Plant Biol 29(3):151–159

    Article  CAS  Google Scholar 

  • Osanai T, Tanaka K (2007) Keeping in touch with PII: PII-interacting proteins in unicellular cyanobacteria. Plant Cell Physiol 48(7):908–914

    Article  CAS  PubMed  Google Scholar 

  • Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605–1612

    Article  CAS  PubMed  Google Scholar 

  • Price GD (2011) Inorganic carbon transporters of the cyanobacterial CO2 concentrating mechanism. Photosynth Res 109(1–3):47–57

    Article  CAS  PubMed  Google Scholar 

  • Price GD, Howitt SM (2010) The cyanobacterial bicarbonate transporter BicA: its physiological role and the implications of structural similarities with human SLC26 transporters. Biochem Cell Biol 89(2):178–188

    Article  Google Scholar 

  • Price GD, Sültemeyer D, Klughammer B, Ludwig M, Badger MR (1998) The functioning of the CO2 concentrating mechanism in several cyanobacterial strains: a review of general physiological characteristics, genes, proteins, and recent advances. Can J Bot 76(6):973–1002

    CAS  Google Scholar 

  • Price GD, Maeda S-I, Omata T, Badger (2002) Modes of active inorganic carbon uptake in the cyanobacterium, Synechococcus sp. PCC7942. Funct Plant Biol 29(3):131–149

    Article  CAS  Google Scholar 

  • Price GD, Woodger FJ, Badger MR, Howitt SM, Tucker L (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci USA 101(52):18228–18233

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Price GD, Badger MR, Woodger FJ, Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59(7):1441–1461

    Article  CAS  PubMed  Google Scholar 

  • Price GD, Badger MR, von Caemmerer S (2011a) The prospect of using cyanobacterial bicarbonate transporters to improve leaf photosynthesis in C3 crop plants. Plant Physiol 155(1):20–26

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Price GD, Shelden MC, Howitt SM (2011b) Membrane topology of the cyanobacterial bicarbonate transporter, SbtA, and identification of potential regulatory loops. Mol Membr Biol 28(5):265–275

    Article  CAS  PubMed  Google Scholar 

  • Rae BD, Forster B, Badger MR, Price GD (2011) The CO2-concentrating mechanism of Synechococcus WH5701 is composed of native and horizontally-acquired components. Photosynth Res 109(1–3):59–72

    Article  CAS  PubMed  Google Scholar 

  • Rae BD, Long BM, Badger MR, Price GD (2013) Functions, compositions, and evolution of the two types of carboxysomes: polyhedral microcompartments that facilitate CO2 fixation in cyanobacteria and some proteobacteria. Microbiol Mol Biol Rev 77(3):357–379

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roberts EW, Cai F, Kerfeld CA, Cannon GC, Heinhorst S (2012) Isolation and characterization of the Prochlorococcus carboxysome reveal the presence of the novel shell protein CsoS1D. J Bacteriol 194(4):787–795

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425

    CAS  PubMed  Google Scholar 

  • Sasaki J, Brown L, Chon Y, Kandori H, Maeda A, Needleman R, Lanyi J (1995) Conversion of bacteriorhodopsin into a chloride ion pump. Science 269(5220):73–75

    Article  CAS  PubMed  Google Scholar 

  • Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, Hess WR, Post AF, Hagemann M, Paulsen I, Partensky F (2009) Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol Rev 73(2):249–299

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schobert B, Lanyi JK (1982) Halorhodopsin is a light-driven chloride pump. J Biol Chem 257(17):10306–10313

    CAS  PubMed  Google Scholar 

  • Shelden MC, Howitt SM, Price GD (2010) Membrane topology of the cyanobacterial bicarbonate transporter, BicA, a member of the SulP (SLC26A) family. Mol Membr Biol 27(1):12–23

    Article  PubMed  Google Scholar 

  • Shibata M, Ohkawa H, Kaneko T, Fukuzawa H, Tabata S, Kaplan A, Ogawa T (2001) Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc Natl Acad Sci USA 98(20):11789–11794

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shibata M, Katoh H, Sonoda M, Ohkawa H, Shimoyama M, Fukuzawa H, Kaplan A, Ogawa T (2002) Genes essential to sodium-dependent bicarbonate transport in cyanobacteria: function and phylogenetic analysis. J Biol Chem 277(21):18658–18664

    Article  CAS  PubMed  Google Scholar 

  • Shih PM, Wu D, Latifi A, Axen SD, Fewer DP, Talla E, Calteau A, Cai F, Tandeau de Marsac N, Rippka R, Herdman M, Sivonen K, Coursin T, Laurent T, Goodwin L, Nolan M, Davenport KW, Han CS, Rubin EM, Eisen JA, Woyke T, Gugger M, Kerfeld CA (2013) Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci USA 110(3):1053–1058

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shih PM, Zarzycki J, Niyogi KK, Kerfeld CA (2014) Introduction of a synthetic CO2-fixing photorespiratory bypass into a cyanobacterium. J Biol Chem 289(14):9493–9500

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shively JM, Ball F, Brown DH, Saunders RE (1973) Functional organelles in prokaryotes: polyhedral inclusions (carboxysomes) of Thiobacillus neapolitanus. Science 182(4112):584–586

    Article  CAS  PubMed  Google Scholar 

  • Spudich JL (1994) Protein-protein interaction converts a proton pump into a sensory receptor. Cell 79(5):747–750

    Article  CAS  PubMed  Google Scholar 

  • Stöckel J, Elvitigala TR, Liberton M, Pakrasi HB (2013) Carbon availability affects diurnally controlled processes and cell morphology of Cyanothece 51142. PLoS ONE 8(2):e56887

    Article  PubMed Central  PubMed  Google Scholar 

  • Takahashi T, Mochizuki Y, Kamo N, Kobatake Y (1985) Evidence that the long-lifetime photointermediate of s-rhodopsin is a receptor for negative phototaxis in Halobacterium halobium. Biochem Biophys Res Commun 127(1):99–105

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tolonen AC, Aach J, Lindell D, Johnson ZI, Rector T, Steen R, Church GM, Chisholm SW (2006) Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability. Mol Syst Biol 2:53

    Article  PubMed Central  PubMed  Google Scholar 

  • Ugalde JA, Podell S, Narasingarao P, Allen EE (2011) Xenorhodopsins, an enigmatic new class of microbial rhodopsins horizontally transferred between archaea and bacteria. Biol Direct 6:52

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Váró G, Brown LS, Needleman R, Lanyi JK (1996) Proton transport by halorhodopsin. Biochemistry 35(21):6604–6611

    Article  PubMed  Google Scholar 

  • Volokita M, Zenvirth D, Kaplan A, Reinhold L (1984) Nature of the inorganic carbon species actively taken up by the cyanobacterium Anabaena variabilis. Plant Physiol 76(3):599–602

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang HL, Postier BL, Burnap RL (2004) Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. J Biol Chem 279(7):5739–5751

    Article  CAS  PubMed  Google Scholar 

  • Wheatley NM, Sundberg CD, Gidaniyan SD, Cascio D, Yeates TO (2014) Structure and identification of a pterin dehydratase-like protein as a RuBisCO assembly factor in the alpha-carboxysome. J Biol Chem 289:7973–7981

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu M, Bernat G, Singh A, Mi H, Rogner M, Pakrasi HB, Ogawa T (2008a) Properties of mutants of Synechocystis sp. strain PCC 6803 lacking inorganic carbon sequestration systems. Plant Cell Physiol 49(11):1672–1677

    Article  CAS  PubMed  Google Scholar 

  • Xu M, Ogawa T, Pakrasi HB, Mi H (2008b) Identification and localization of the CupB protein involved in constitutive CO2 uptake in the cyanobacterium, Synechocystis sp. strain PCC 6803. Plant Cell Physiol 49(6):994–997

    Article  PubMed  Google Scholar 

  • Zarzycki J, Axen SD, Kinney JN, Kerfeld CA (2013) Cyanobacterial-based approaches to improving photosynthesis in plants. J Exp Bot 64(3):787–798

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Battchikova N, Jansen T, Appel J, Ogawa T, Aro EM (2004) Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp. PCC 6803. Plant Cell 16(12):3326–3340

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang P, Battchikova N, Paakkarinen V, Katoh H, Iwai M, Ikeuchi M, Pakrasi HB, Ogawa T, Aro EM (2005) Isolation, subunit composition and interaction of the NDH-1 complexes from Thermosynechococcus elongatus BP-1. Biochem J 390(Pt 2):513–520

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank Ryan L. Leverenz, Onur Erbilgin, and Seth D. Axen for helpful discussions. This work was supported by the NSF (EF1105892 and MCB0851094) and by the US DOE contract no. DE-AC02 05CH11231.

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Authors and Affiliations

  1. DOE Plant Research Laboratories, Department of Biochemistry and Molecular Biology, Michigan State University, 612 Wilson Road, East Lansing, MI, 48824, USA

    Sandeep B. Gaudana, Jan Zarzycki & Cheryl A. Kerfeld

  2. Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA

    Jan Zarzycki & Cheryl A. Kerfeld

  3. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA, 94598, USA

    Vamsi K. Moparthi

  4. Department of Plant and Microbial Biology, University of California, Berkeley, CA, 94720, USA

    Cheryl A. Kerfeld

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  1. Sandeep B. Gaudana
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  2. Jan Zarzycki
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  4. Cheryl A. Kerfeld
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Correspondence to Cheryl A. Kerfeld.

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Sandeep B. Gaudana and Jan Zarzycki contributed equally.

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Gaudana, S.B., Zarzycki, J., Moparthi, V.K. et al. Bioinformatic analysis of the distribution of inorganic carbon transporters and prospective targets for bioengineering to increase Ci uptake by cyanobacteria. Photosynth Res 126, 99–109 (2015). https://doi.org/10.1007/s11120-014-0059-8

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