Biofuels from cyanobacteria -a metabolic engineering approach
DOI:
https://doi.org/10.14719/pst.2505Keywords:
Biofuel production, CRISPR, cyanobacteria, genetic engineering, genes, secondary metabolitesAbstract
The concern about the limited availability of petroleum-based fuels and their role in increasing CO2 levels in the atmosphere has sparked significant attention toward biofuel and bioenergy production. The global pursuit of sustainable energy sources has catalyzed innovative research into alternative biofuel production strategies. Transforming CO2 into usable fuels and chemicals is gaining even more prominence. Cyanobacteria, renowned for their photosynthetic ability, have emerged as promising candidates for biofuel synthesis. Their ability to convert solar energy and carbon dioxide into valuable biofuels makes them a compelling avenue for sustainable energy solutions. Using metabolic engineering principles, researchers have endeavored to optimize cyanobacterial metabolic pathways, enhance photosynthetic efficiency, and redirect carbon flux toward biofuel precursors. Numerous species of cyanobacteria offer genetic and metabolic traits that facilitate manipulation, and their photosynthetic characteristics imply that carbohydrates, fatty acids, and even alcohol could serve as potential renewable sources for biofuels. This review showcases cyanobacteria's ability as a biofuel source and emphasizes the transformative influence of metabolic engineering employed in the creation and production of "cyanofuels”
Downloads
References
Sharma NK, Tiwari SP, Tripathi K, Rai AK. Sustainability and cyanobacteria (blue-green algae): facts and challenges. Journal of Applied Phycology. 2011;23:1059-81. https://doi.org/10.1007/s10811-010-9626-3
Chaib S, Pistevos JC, Bertrand C, Bonnard I. Allelopathy and allelochemicals from microalgae: An innovative source for bio-herbicidal compounds and biocontrol research. Algal Research. 2021 Apr 1;54:102213. https://doi.org/10.1016/j.algal.2021.102213
Jareonsin S, Pumas C. Advantages of heterotrophic microalgae as a host for phytochemicals production. Frontiers in Bioengineering and Biotechnology. 2021;9:628597. https://doi.org/10.3389/fbioe.2021.628597
Anahas AM, Muralitharan G. Characterization of heterocystous cyanobacterial strains for biodiesel production based on fatty acid content analysis and hydrocarbon production. Energy Conversion and Management. 2018;157:423-37. https://doi.org/10.1016/j.enconman.2017.12.012
Sivaramakrishnan R, Suresh S, Kanwal S, Ramadoss G, Ramprakash B, Incharoensakdi A. Microalgal biorefinery concepts’ developments for biofuel and bioproducts: Current perspective and bottlenecks. International Journal of Molecular Sciences. 2022;23(5):2623. https://doi.org/10.3390/ijms23052623
Singh SP, Pathak J, Sinha RP. Cyanobacterial factories for the production of green energy and value-added products: An integrated approach for economic viability. Renewable and Sustainable Energy Reviews. 2017;69:578-95. https://doi.org/10.1016/j.rser.2016.11.110
Pathak J, Rajneesh, Maurya PK, Singh SP, Haeder DP, Sinha RP. Cyanobacterial farming for environment friendly sustainable agriculture practices: innovations and perspectives. Frontiers in Environmental Science. 2018;6:7. https://doi.org/10.3389/fenvs.2018.00007
Parmar A, Singh NK, Pandey A, Gnansounou E, Madamwar D. Cyanobacteria and microalgae: a positive prospect for biofuels. Bioresource technology. 2011;102(22):10163-72. https://doi.org/10.1016/j.biortech.2011.08.030
Savakis P, Hellingwerf KJ. Engineering cyanobacteria for direct biofuel production from CO2. Current opinion in biotechnology. 2015;33:8-14. https://doi.org/10.1016/j.copbio.2014.09.007
Quintana N, Van der Kooy F, Van de Rhee MD, Voshol GP, Verpoorte R. Renewable energy from Cyanobacteria: energy production optimization by metabolic pathway engineering. Applied microbiology and biotechnology. 2011;91:471-90. https://doi.org/10.1007/s00253-011-3394-0
Emamalipour M, Seidi K, Zununi Vahed S, Jahanban-Esfahlan A, Jaymand M, Majdi H, Amoozgar Z, Chitkushev LT, Javaheri T, Jahanban-Esfahlan R, Zare P. Horizontal gene transfer: from evolutionary flexibility to disease progression. Frontiers in cell and developmental biology. 2020;8:229. https://doi.org/10.3389/fcell.2020.00229
Andrews F, Faulkner M, Toogood HS, Scrutton NS. Combinatorial use of environmental stresses and genetic engineering to increase ethanol titres in cyanobacteria. Biotechnology for Biofuels. 2021;14(1):240. https://doi.org/10.1186/s13068-021-02091-w
de Farias Silva CE, Bertucco A. Bioethanol from microalgae and cyanobacteria: a review and technological outlook. Process Biochemistry. 2016;51(11):1833-42. https://doi.org/10.1016/j.procbio.2016.02.016
Mandal S, Rath J. Extremophilic cyanobacteria for novel drug development. Springer; 2014.
Demay J, Bernard C, Reinhardt A, Marie B. Natural products from cyanobacteria: Focus on beneficial activities. Marine drugs. 2019;17(6):320. https://doi.org/10.3390/md17060320
Dittmann E, Gugger M, Sivonen K, Fewer DP. Natural product biosynthetic diversity and comparative genomics of the cyanobacteria. Trends in microbiology. 2015;23(10):642-52. https://doi.org/10.1016/j.tim.2015.07.008
Taiz L, Zeiger E. Chapter 12: Assimilation of mineral nutrients. Plant Physiology, 4th ed.; Sinauer Associates, Inc.: Sunderland, MA, USA. 2006:265-6.
Vijay D, Akhtar MK, Hess WR. Genetic and metabolic advances in the engineering of cyanobacteria. Current opinion in biotechnology. 2019;59:150-6. https://doi.org/10.1016/j.copbio.2019.05.012
Taton A, Ecker A, Diaz B, Moss NA, Anderson B, Reher R, Leao TF, Simkovsky R, Dorrestein PC, Gerwick L, Gerwick WH. Heterologous expression of cryptomaldamide in a cyanobacterial host. ACS synthetic biology. 2020;9(12):3364-76. https://doi.org/10.1021/acssynbio.0c00431
Zhang R, Xu W, Shao S, Wang Q. Gene silencing through CRISPR interference in bacteria: current advances and future prospects. Frontiers in Microbiology. 2021;12:635227. https://doi.org/10.3389/fmicb.2021.635227
Ongley SE, Bian X, Zhang Y, Chau R, Gerwick WH, Mu?ller R, Neilan BA. High-titer heterologous production in E. coli of lyngbyatoxin, a protein kinase C activator from an uncultured marine cyanobacterium. ACS chemical biology. 2013;8(9):1888-93. https://doi.org/10.1021/cb400189j
Park SH, Lee K, Jang JW, Hahn JS. Metabolic engineering of Saccharomyces cerevisiae for production of shinorine, a sunscreen material, from xylose. ACS Synthetic Biology. 2018 ;8(2):346-57. https://doi.org/10.1021/acssynbio.8b00388
Kudoh K, Kawano Y, Hotta S, Sekine M, Watanabe T, Ihara M. Prerequisite for highly efficient isoprenoid production by cyanobacteria discovered through the over-expression of 1-deoxy-d-xylulose 5-phosphate synthase and carbon allocation analysis. Journal of bioscience and bioengineering. 2014;118(1):20-8. https://doi.org/10.1016/j.jbiosc.2013.12.018
Gao X, Gao F, Liu D, Zhang H, Nie X, Yang C. Engineering the methylerythritol phosphate pathway in cyanobacteria for photosynthetic isoprene production from CO2. Energy & Environmental Science. 2016;9(4):1400-11. https://doi.org/10.1039/C5EE03102H
Lai MJ, Lan EI. Photoautotrophic synthesis of butyrate by metabolically engineered cyanobacteria. Biotechnology and Bioengineering. 2019;116(4):893-903. https://doi.org/10.1002/bit.26903
Sarnaik A, Abernathy MH, Han X, Ouyang Y, Xia K, Chen Y, Cress B, Zhang F, Lali A, Pandit R, Linhardt RJ. Metabolic engineering of cyanobacteria for photoautotrophic production of heparosan, a pharmaceutical precursor of heparin. Algal Research. 2019 Jan 1;37:57-63. https://doi.org/10.1016/j.algal.2018.11.010
Chin T, Okuda Y, Ikeuchi M. Improved sorbitol production and growth in cyanobacteria using promiscuous haloacid dehalogenase-like hydrolase. Journal of Biotechnology. 2019;306:100002. https://doi.org/10.1016/j.btecx.2019.100002
Fan ES, Lu KW, Wen RC, Shen CR. Photosynthetic reduction of xylose to xylitol using cyanobacteria. Biotechnology Journal. 2020;15(6):1900354. https://doi.org/10.1002/biot.201900354
Diao J, Song X, Zhang L, Cui J, Chen L, Zhang W. Tailoring cyanobacteria as a new platform for highly efficient synthesis of astaxanthin. Metabolic Engineering. 2020;61:275-87. https://doi.org/10.1016/j.ymben.2020.07.003
Choi SY, Woo HM. CRISPRi-dCas12a: a dCas12a-mediated CRISPR interference for repression of multiple genes and metabolic engineering in cyanobacteria. ACS synthetic biology. 2020;9(9):2351-61. https://doi.org/10.1021/acssynbio.0c00091
Verma S, Thapa S, Siddiqui N, Chakdar H. Cyanobacterial secondary metabolites towards improved commercial significance through multiomics approaches. World Journal of Microbiology and Biotechnology. 2022;38(6):100. https://doi.org/10.1007/s11274-022-03285-6
Cheng J, Zhang K, Hou Y. The current situations and limitations of genetic engineering in cyanobacteria: a mini review. Molecular Biology Reports. 2023;29:1-7. https://doi.org/10.1007/s11033-023-08456-8
Wendt KE, Pakrasi HB. Genomics approaches to deciphering natural transformation in cyanobacteria. Frontiers in Microbiology. 2019;10:1259. https://doi.org/10.3389/fmicb.2019.01259
Stucken K, Koch R, Dagan T. Cyanobacterial defense mechanisms against foreign DNA transfer and their impact on genetic engineering. Biological research. 2013;46(4):373-82. http://dx.doi.org/10.4067/S0716-97602013000400009
Nies F, Mielke M, Pochert J, Lamparter T. Natural transformation of the filamentous cyanobacterium Phormidium lacuna. PLoS One. 2020;15(6):e0234440. https://doi.org/10.1371/journal.pone.0234440
Yerrapragada S, Siefert JL, Fox GE. Horizontal gene transfer in cyanobacterial signature genes. Horizontal Gene Transfer: Genomes in Flux. 2009;339-66. https://doi.org/10.1007/978-1-60327-853-9_20
Opel F, Axmann IM, Klahn S. The Molecular Toolset and Techniques Required to Build Cyanobacterial Cell Factories. Springer, Cham. 2022 https://doi.org/10.1007/10_2022_210
Rai KK, Rai R, Singh S, Rai LC. Synthetic Biology Tools in Cyanobacterial Biotechnology: Recent Developments and Opportunities. Re-visiting the Rhizosphere Eco-system for Agricultural Sustainability. 2022:181-203. https://doi.org/10.1007/978-981-19-4101-6_10
Ducat DC, Way JC, Silver PA. Engineering cyanobacteria to generate high-value products. Trends in biotechnology. 2011;29(2):95-103. https://doi.org/10.1016/j.tibtech.2010.12.003
Zhou J, Li Y. Engineering cyanobacteria for fuels and chemicals production. Protein & cell. 2010;1(3):207-10. https://doi.org/10.1007/s13238-010-0043-9
Khan AZ, Bilal M, Mehmood S, Sharma A, Iqbal HM. State-of-the-art genetic modalities to engineer cyanobacteria for sustainable biosynthesis of biofuel and fine chemicals to meet bio–economy challenges. Life. 2019;9(3):54. https://doi.org/10.3390/life9030054
Takahama K, Matsuoka M, Nagahama K, Ogawa T. Construction and analysis of a recombinant cyanobacterium expressing a chromosomally inserted gene for an ethylene-forming enzyme at the psbAI locus. Journal of bioscience and bioengineering. 2003;95(3):302-5. https://doi.org/10.1016/S1389-1723(03)80034-8
Guerrero F, Carbonell V, Cossu M, Correddu D, Jones PR. Ethylene synthesis and regulated expression of recombinant protein in Synechocystis sp. PCC 6803. PloS one. 2012 Nov 21;7(11):e50470. https://doi.org/10.1371/journal.pone.0050470
Jindou S, Ito Y, Mito N, Uematsu K, Hosoda A, Tamura H. Engineered platform for bioethylene production by a cyanobacterium expressing a chimeric complex of plant enzymes. ACS synthetic biology. 2014;3(7):487-96. https://doi.org/10.1021/sb400197f
Tan X, Du W, Lu X. Photosynthetic and extracellular production of glucosylglycerol by genetically engineered and gel-encapsulated cyanobacteria. Applied microbiology and biotechnology. 2015;99:2147-54. https://doi.org/10.1007/s00253-014-6273-7
Rahman A, Prihantini NB, Nasruddin N. Fatty acid of microalgae as a potential feedstock for biodiesel production in Indonesia. In: AIP Conference Proceedings 2019 (Vol. 2062, No. 1). AIP Publishing. https://doi.org/10.1063/1.5086606
Tarin NJ, Ali NM, Chamon AS, Mondol MN, Rahman MM, Aziz A. Optimizing Chlorella vulgaris and Anabaena variabilis Growth Conditions for Use as Biofuel Feedstock. Journal of the Asiatic Society of Bangladesh, Science. 2016;42(2):191-200.
Moraes LE, Blow MJ, Hawley ER, Piao H, Kuo R, Chiniquy J, Shapiro N, Woyke T, Fadel JG, Hess M. Resequencing and annotation of the Nostoc punctiforme ATTC 29133 genome: facilitating biofuel and high-value chemical production. AMB Express. 2017;7:1-9. https://doi.org/10.1186/s13568-017-0338-9
Trejo M, Mejica GF, Saetang N, Lomlai P. Exploration of fatty acid methyl esters (FAME) in cyanobacteria for a wide range of algae-based biofuels. Maejo International Journal of Energy and Environmental Communication. 2020;2(3):35-42. https://doi.org/10.54279/mijeec.v2i3.245039
Kushwaha D, Saha S, Dutta S. Enhanced biomass recovery during phycoremediation of Cr (VI) using cyanobacteria and prospect of biofuel production. Industrial & Engineering Chemistry Research. 2014;53(51):19754-64. https://doi.org/10.1021/ie501311c
Ruffing AM. Engineered cyanobacteria: teaching an old bug new tricks. Bioengineered bugs. 2011;2(3):136-49. https://doi.org/10.4161/bbug.2.3.15285
Parwani L, Bhatt M, Singh J. Potential biotechnological applications of cyanobacterial exopolysaccharides. Brazilian Archives of Biology and Technology. 2021;64:e21200401.
Zymanczyk-Duda E, Samson SO, Brzezinska-Rodak M, Klimek-Ochab M. Versatile applications of cyanobacteria in biotechnology. Microorganisms. 2022;10(12):2318. https://doi.org/10.3390/microorganisms10122318
Farrokh P, Sheikhpour M, Kasaeian A, Asadi H, Bavandi R. Cyanobacteria as an eco?friendly resource for biofuel production: a critical review. Biotechnology progress. 2019;35(5):e2835. https://doi.org/10.1002/btpr.2835
Gharabaghi M, Delavai Amrei H, Moosavi Zenooz A, Shahrivar Guzullo J, Zokaee Ashtiani F. Biofuels: bioethanol, biodiesel, biogas, biohydrogen from plants and microalgae. CO2 Sequestration, Biofuels and Depollution. 2015:233-74. https://doi.org/10.1007/978-3-319-11906-9_6
Roussou S, Albergati A, Liang F, Lindblad P. Engineered cyanobacteria with additional overexpression of selected Calvin-Benson-Bassham enzymes show further increased ethanol production. Metabolic engineering communications. 2021;12:e00161. https://doi.org/10.1016/j.mec.2021.e00161
Afrin S, Khan MR, Zhang W, Wang Y, Zhang W, He L, Ma G. Membrane-located expression of thioesterase from Acinetobacter baylyi enhances free fatty acid production with decreased toxicity in Synechocystis sp. PCC6803. Frontiers in microbiology. 2018;9:2842. https://doi.org/10.3389/fmicb.2018.02842
Kaczmarzyk D, Cengic I, Yao L, Hudson EP. Diversion of the long-chain acyl-ACP pool in Synechocystis to fatty alcohols through CRISPRi repression of the essential phosphate acyltransferase PlsX. Metabolic engineering. 2018;45:59-66. https://doi.org/10.1016/j.ymben.2017.11.014
Yunus IS, Wichmann J, Wordenweber R, Lauersen KJ, Kruse O, Jones PR. Synthetic metabolic pathways for photobiological conversion of CO2 into hydrocarbon fuel. Metabolic Engineering. 2018;49:201-11. https://doi.org/10.1016/j.ymben.2018.08.008
Chaves JE, Rueda-Romero P, Kirst H, Melis A. Engineering isoprene synthase expression and activity in cyanobacteria. ACS synthetic biology. 2017;6(12):2281-92. https://doi.org/10.1021/acssynbio.7b00214
Lin PC, Zhang F, Pakrasi HB. Enhanced limonene production in a fast-growing cyanobacterium through combinatorial metabolic engineering. Metabolic Engineering Communications. 2021;12:e00164. https://doi.org/10.1016/j.mec.2021.e00164
Lee HJ, Lee J, Lee SM, Um Y, Kim Y, Sim SJ, Choi JI, Woo HM. Direct conversion of CO2 to ?-farnesene using metabolically engineered Synechococcus elongatus PCC 7942. Journal of agricultural and food chemistry. 2017;65(48):10424-8. https://doi.org/10.1021/acs.jafc.7b03625
Oliver JW, Machado IM, Yoneda H, Atsumi S. Combinatorial optimization of cyanobacterial 2, 3-butanediol production. Metabolic Engineering. 2014 Mar 1;22:76-82. https://doi.org/10.1016/j.ymben.2014.01.001
Hirokawa Y, Kubo T, Soma Y, Saruta F, Hanai T. Enhancement of acetyl-CoA flux for photosynthetic chemical production by pyruvate dehydrogenase complex overexpression in Synechococcus elongatus PCC 7942. Metabolic engineering. 2020;57:23-30. https://doi.org/10.1016/j.ymben.2019.07.012
Liu X, Miao R, Lindberg P, Lindblad P. Modular engineering for efficient photosynthetic biosynthesis of 1-butanol from CO 2 in cyanobacteria. Energy and Environmental Science. 2019;12(9):2765-77. 10.1039/C9EE01214A
Aboim JB, Oliveira D, Ferreira JE, Siqueira AS, Dall'Agnol LT, Rocha Filho GN, Gonçalves EC, Nascimento LA. Determination of biodiesel properties based on a fatty acid profile of eight Amazon cyanobacterial strains grown in two different culture media. RSC advances. 2016;6(111):109751-8. https://doi.org/10.1039/C6RA23268J
Aboim JB, Oliveira DT, Mescouto VA, Dos Reis AS, da Rocha Filho GN, Santos AV, Xavier LP, Santos AS, Goncalves EC, do Nascimento LA. Optimization of light intensity and NaNO3 concentration in Amazon cyanobacteria cultivation to produce biodiesel. Molecules. 2019;24(12):2326. https://doi.org/10.3390/molecules24122326
Liu X, Curtiss III R. Thermorecovery of cyanobacterial fatty acids at elevated temperatures. Journal of biotechnology. 2012;161(4):445-9. https://doi.org/10.1016/j.jbiotec.2012.08.013
Santos-Merino M, Garcillan-Barcia MP, de la Cruz F. Engineering the fatty acid synthesis pathway in Synechococcus elongatus PCC 7942 improves omega-3 fatty acid production. Biotechnology for biofuels. 2018;11(1):1-3. https://doi.org/10.1186/s13068-018-1243-4
de Oliveira DT, Vasconcelos CT, Feitosa AM, Aboim JB, de Oliveira AD, Xavier LP, Santos AS, Goncalves EC, da Rocha Filho GN, do Nascimento LA. Lipid profile analysis of three new Amazonian cyanobacteria as potential sources of biodiesel. Fuel. 2018;234:785-8. https://doi.org/10.1016/j.fuel.2018.07.080
Nithiya K, Subramanian P, Praveen Kumar D, Komalabharathi P, Karuppasamy Vikraman V. Bio-Oil: A Green
Biofuel. In: Baskar C, Ramakrishna S, Daniela La Rosa A. (eds) Encyclopedia of Green Materials. Springer, Singapore 2022.
Hu Z, Zheng Y, Yan F, Xiao B, Liu S. Bio-oil production through pyrolysis of blue-green algae blooms (BGAB): Product distribution and bio-oil characterization. Energy. 2013;52:119-25. https://doi.org/10.1016/j.energy.2013.01.059
Sivaramakrishnan R, Incharoensakdi A. Cyanobacteria as renewable sources of bioenergy (biohydrogen, bioethanol, and bio-oil production). In: Ecophysiology and biochemistry of cyanobacteria. Singapore: Springer Nature Singapore. 2022. https://doi.org/10.1007/978-981-16-4873-1_19
Sitther V, Tabatabai B, Fathabad SG, Gichuki S, Chen H, Arumanayagam AC. Cyanobacteria as a biofuel source: advances and applications. Advances in Cyanobacterial Biology. 2020:269-89. https://doi.org/10.1016/B978-0-12-819311-2.00018-8
Converti A, Oliveira RP, Torres BR, Lodi A, Zilli M. Biogas production and valorization by means of a two-step biological process. Bioresource technology. 2009;100(23):5771-6. https://doi.org/10.1016/j.biortech.2009.05.072
Zaki MA, Ashour M, Heneash AM, Mabrouk MM, Alprol AE, Khairy HM, Nour AM, Mansour AT, Hassanien HA, Gaber A, Elshobary ME. Potential Applications of native cyanobacterium isolate (Arthrospira platensis NIOF17/003) for biodiesel production and utilization of its byproduct in marine rotifer (Brachionus plicatilis) production. Sustainability. 2021;13(4):1769. https://doi.org/10.3390/su13041769
Wendt KE, Ungerer J, Cobb RE, Zhao H, Pakrasi HB. CRISPR/Cas9 mediated targeted mutagenesis of the fast-growing cyanobacterium Synechococcus elongatus UTEX 2973. Microbial cell factories. 2016;15:1-8. https://doi.org/10.1186/s12934-016-0514-7
Higo A and Ehira S. Spatiotemporal gene repression system in the heterocyst-forming multicellular cyanobacterium Anabaena sp. PCC 7120. ACS Synth Biol. 2019;8(4):641–646. https://doi.org/10.1021/acssynbio.8b00496
Wang F, Gao Y, Yang G. Recent advances in synthetic biology of cyanobacteria for improved chemicals production. Bioengineered. 2020;11(1):1208-20. https://doi.org/10.1080/21655979.2020.1837458
Li H, Shen CR, Huang CH, Sung LY, Wu MY, Hu YC. CRISPR-Cas9 for the genome engineering of cyanobacteria and succinate production. Metabolic engineering. 2016;38:293-302. https://doi.org/10.1016/j.ymben.2016.09.006
Ungerer J, Pakrasi HB. Cpf1 is a versatile tool for CRISPR genome editing across diverse species of cyanobacteria. Scientific reports. 2016;6(1):39681. https://doi.org/10.1038/srep39681
Downloads
Published
Versions
- 22-12-2023 (2)
- 10-11-2023 (1)
How to Cite
Issue
Section
License
Copyright (c) 2022 P Pooja, K Edison Lekshmi, Pradeep N S
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright and Licence details of published articles
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
Open Access Policy
Plant Science Today is an open access journal. There is no registration required to read any article. All published articles are distributed under the terms of the Creative Commons Attribution License (CC Attribution 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited (https://creativecommons.org/licenses/by/4.0/). Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
