Exploiting AGPase genes and encoded proteins to prioritize development of optimum engineered strains in microalgae towards sustainable biofuel production.

AGPase Comparative genomics Lipid productivity Microalgae Structural biology Sustainable biofuel

Journal

World journal of microbiology & biotechnology
ISSN: 1573-0972
Titre abrégé: World J Microbiol Biotechnol
Pays: Germany
ID NLM: 9012472

Informations de publication

Date de publication:
27 May 2023
Historique:
received: 21 04 2022
accepted: 18 05 2023
medline: 29 5 2023
pubmed: 27 5 2023
entrez: 26 5 2023
Statut: epublish

Résumé

Although ADP glucose pyrophosphorylase (AGPase), with two large subunits (ls) and two small subunits (ss), is a promising knockout target for increasing the neutral lipid content, the details regarding the sequence-structure features and their distribution within metabolic system in microalgae is rather limited. Against this backdrop, a comprehensive genome-wide comparative analysis on 14 sequenced microalgal genomes was performed. For the first time the heterotetrameric structure of the enzyme and the interaction of the catalytic unit with the substrate was also studied. Novel findings of the present study includes: (i) at the DNA level, the genes controlling the ss are more conserved than those controlling the ls; the variation in both the gene groups is mainly due to exon number, exon length and exon phase distribution; (ii) at protein level, the ss genes are more conserved relative to those for ls; (III) three putative key consensus sequences 'LGGGAGTRLYPLTKNRAKPAV', 'WFQGTADAV' and 'ASMGIYVFRKD' were ubiquitously conserved in all the AGPases; (iv) molecular dynamics investigations revealed that the modeled AGPase heterotetrameric structure, from oleaginous algae Chlamydomonas reinharditii, was completely stable in real time environment; (v) The binding interfaces of catalytic unit, ssAGPase, from C. reinharditii with α-D-glucose 1-phosphate (αGP) was also analyzed. The results of the present study have provided system-based insights into the structure-function of the genes and encoded proteins, which provided clues for exploitation of variability in these genes that, could be further utilized to design site-specific mutagenic experiments for engineering of microalgal strains towards sustainable development of biofuel.

Identifiants

pubmed: 37237168
doi: 10.1007/s11274-023-03654-9
pii: 10.1007/s11274-023-03654-9
doi:

Substances chimiques

Glucose-1-Phosphate Adenylyltransferase EC 2.7.7.27
Biofuels 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

209

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Alishah Aratboni H, Rafiei N, Garcia-Granados R, Alemzadeh A, Morones-Ramírez JR (2019) Biomass and lipid induction strategies in microalgae for biofuel production and other applications. Microb Cell Fact 18(1):1–17
Araújo R, Vázquez Calderón F, Sánchez López J, Azevedo IC, Bruhn A, Fluch S, Ullmann J (2021) Current status of the algae production industry in Europe: an emerging sector of the Blue Bioeconomy. Front Mar Sci 7:1247
Arora N, Philippidis GP (2021) Insights into the physiology of Chlorella vulgaris cultivated in sweet sorghum bagasse hydrolysate for sustainable algal biomass and lipid production. Sci Rep 11(1):1–14
Arora N, Yen HW, Philippidis GP (2020) Harnessing the power of mutagenesis and adaptive laboratory evolution for high lipid production by oleaginous microalgae and yeasts. Sustainability 12(12):5125
Barıs I, Tuncel A, Ozber N, Keskin O, Kavakli IH (2009) Investigation of the interaction between the large and small subunits of potato ADP-glucose pyrophosphorylase. PLoS Comput Biol 5(10):e1000546
pubmed: 19876371 pmcid: 2759521
Batra R, Saripalli G, Mohan A, Gupta S, Gill KS, Varadwaj PK, Gupta PK (2017) Comparative analysis of AGPase genes and encoded proteins in eight monocots and three dicots with emphasis on wheat. Front Plant Sci 8:19
pubmed: 28174576 pmcid: 5259687
Blaby IK, Glaesener AG, Mettler T, Fitz-Gibbon ST, Gallaher SD, Liu B, Merchant SS (2013) Systems-level analysis of nitrogen starvation–induced modifications of carbon metabolism in a Chlamydomonas reinhardtii starchless mutant. Plant Cell 25(11):4305–4323
pubmed: 24280389 pmcid: 3875720
Bowers KJ, Chow DE, Xu H, Dror RO, Eastwood MP, Gregersen BA, Shaw DE (2006). Scalable algorithms for molecular dynamics simulations on commodity clusters. In: SC'06: Proceedings of the 2006 ACM/IEEE Conference on Supercomputing. IEEE. pp. 43–43
Chang KS, Kim J, Park H, Hong SJ, Lee CG, Jin E (2020) Enhanced lipid productivity in AGP knockout marine microalga Tetraselmis sp. using a DNA-free CRISPR-Cas9 RNP method. Bioresource technology 303:122932
pubmed: 32058903
Cho YG, Kang KK (2020) Functional analysis of starch metabolism in plants. Plants 9(9):1152
pubmed: 32899939 pmcid: 7569781
Chu WL (2017) Strategies to enhance production of microalgal biomass and lipids for biofuel feedstock. Eur J Phycol 52(4):419–437
Chu KL, Jenkins LM, Bailey SR, Kambhampati S, Koley S, Foley K, Allen DK (2020) Shifting carbon flux from non-transient starch to lipid allows oil accumulation in transgenic tobacco leaves. BioRxiv.
Cifuente JO, Comino N, Madariaga-Marcos J, López-Fernández S, García-Alija M, Agirre J, Guerin ME (2016) Structural basis of glycogen biosynthesis regulation in bacteria. Structure 24(9):1613–1622
pubmed: 27545622
de Jaeger L, Verbeek RE, Draaisma RB, Martens DE, Springer J, Eggink G, Wijffels RH (2014) Superior triacylglycerol (TAG) accumulation in starchless mutants of Scenedesmus obliquus:(I) mutant generation and characterization. Biotechnol Biofuels 7(1):1–11
Durrett TP, Weise SE, Benning C (2011) Increasing the energy density of vegetative tissues by diverting carbon from starch to oil biosynthesis in transgenic Arabidopsis. Plant Biotechnol J 9(8):874–883
pubmed: 22003502
Eswar N, John B, Mirkovic N, Fiser A, Ilyin VA, Pieper U, Sali A (2003) Tools for comparative protein structure modeling and analysis. Nucleic Acids Res 31(13):3375–3380
pubmed: 12824331 pmcid: 168950
Ferrero DM, Piattoni CV, Asencion Diez MD, Rojas BE, Hartman MD, Ballicora MA, Iglesias AA (2020) Phosphorylation of ADP-glucose pyrophosphorylase during wheat seeds development. Front Plant Sci 11:1058
pubmed: 32754189 pmcid: 7366821
Goodenough U, Blaby I, Casero D, Gallaher SD, Goodson C, Johnson S, Wulan T (2014) The path to triacylglyceride obesity in the sta6 strain of Chlamydomonas reinhardtii. Eukaryot Cell 13(5):591–613
pubmed: 24585881 pmcid: 4060482
Hossain N, Mahlia TMI, Saidur R (2019) Latest development in microalgae-biofuel production with nano-additives. Biotechnol Biofuels 12(1):1–16
Jin X, Ballicora MA, Preiss J, Geiger JH (2005) Crystal structure of potato tuber ADP-glucose pyrophosphorylase. EMBO J 24(4):694–704
pubmed: 15692569 pmcid: 549618
Kato Y, Oyama T, Inokuma K, Vavricka CJ, Matsuda M, Hidese R, Kondo A (2021) Enhancing carbohydrate repartitioning into lipid and carotenoid by disruption of microalgae starch debranching enzyme. Commun Biol 4(1):1–11
Khanum F, Giwa A, Nour M, Al-Zuhair S, Taher H (2020) Improving the economic feasibility of biodiesel production from microalgal biomass via high-value products coproduction. Int J Energy Res 44(14):11453–11472
Koo KM, Jung S, Lee BS, Kim JB, Jo YD, Choi HI, Ahn JW (2017) The mechanism of starch over-accumulation in Chlamydomonas reinhardtii high-starch mutants identified by comparative transcriptome analysis. Front Microbiol 8:858
pubmed: 28588557 pmcid: 5440458
Kumar G, Shekh A, Jakhu S, Sharma Y, Kapoor R, Sharma TR (2020) Bioengineering of microalgae: recent advances, perspectives, and regulatory challenges for industrial application. Front Bioeng Biotechnol 8:914
pubmed: 33014997 pmcid: 7494788
Li Y, Han D, Hu G, Dauvillee D, Sommerfeld M, Ball S, Hu Q (2010a) Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol. Metab Eng 12(4):387–391
pubmed: 20172043
Li Y, Han D, Hu G, Sommerfeld M, Hu Q (2010b) Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii. Biotechnol Bioeng 107(2):258–268
pubmed: 20506159
Li N, Zhang S, Zhao Y, Li B, Zhang J (2011) Over-expression of AGPase genes enhances seed weight and starch content in transgenic maize. Planta 233(2):241–250
pubmed: 20978801
Li T, Gargouri M, Feng J, Park JJ, Gao D, Miao C, Chen S (2015) Regulation of starch and lipid accumulation in a microalga Chlorella sorokiniana. Biores Technol 180:250–257
Lin X, Kaul S, Rounsley S, Shea TP, Benito MI, Town CD, Venter JC (1999) Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402(6763):761–768
pubmed: 10617197
Meier A, Söding J (2015) Automatic prediction of protein 3D structures by probabilistic multi-template homology modeling. PLoS Comput Biol 11(10):e1004343
pubmed: 26496371 pmcid: 4619893
Morales-Sánchez D, Kyndt J, Ogden K, Martinez A (2016) Toward an understanding of lipid and starch accumulation in microalgae: A proteomic study of Neochloris oleoabundans cultivated under N-limited heterotrophic conditions. Algal Res 20:22–34
Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ (2009) AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. J Comput Chem 30(16):2785–2791
pubmed: 19399780 pmcid: 2760638
Mulgund A (2022) Increasing lipid accumulation in microalgae through environmental manipulation, metabolic and genetic engineering: a review in the energy NEXUS framework. Energy Nexus, 100054.
Mutanda T, Naidoo D, Bwapwa JK, Anandraj A (2020) Biotechnological applications of microalgal oleaginous compounds: current trends on microalgal bioprocessing of products. Front Energy Res 299.
Nakata PA, Greene TW, Anderson JM, Smith-White BJ, Okita TW, Preiss J (1991) Comparison of the primary sequences of two potato tuber ADP-glucose pyrophosphorylase subunits. Plant Mol Biol 17(5):1089–1093
pubmed: 1657244
Pelissier MC, Lesley SA, Kuhn P, Bourne Y (2010) Structural insights into the catalytic mechanism of bacterial guanosine-diphospho-D-mannose pyrophosphorylase and its regulation by divalent ions. J Biol Chem 285(35):27468–27476
pubmed: 20573954 pmcid: 2930745
Qu J, Xu S, Zhang Z, Chen G, Zhong Y, Liu L, Guo D (2018) Evolutionary, structural and expression analysis of core genes involved in starch synthesis. Sci Rep 8(1):1–16
Raetz CR, Roderick SL (1995) A left-handed parallel β helix in the structure of UDP-N-acetylglucosamine acyltransferase. Science 270(5238):997–1000
pubmed: 7481807
Rafa N, Ahmed SF, Badruddin IA, Mofijur M, Kamangar S (2021) Strategies to produce cost-effective third-generation biofuel from microalgae. Front Energy Res 9:1–11
Rawat J, Gupta PK, Pandit S, Priya K, Agarwal D, Pant M, Pande V (2022) Latest expansions in lipid enhancement of microalgae for biodiesel production: an update. Energies 15(4):1550
Rook F, Corke F, Card R, Munz G, Smith C, Bevan MW (2001) Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signalling. Plant J 26(4):421–433
pubmed: 11439129
Sahoo S, Mahapatra SR, Das N, Parida BK, Rath S, Misra N, Suar M (2020a) Functional elucidation of hypothetical proteins associated with lipid accumulation: Prioritizing genetic engineering targets for improved algal biofuel production. Algal Res 47:101887
Sahoo S, Mahapatra SR, Parida BK, Narang PK, Rath S, Misra N, Suar M (2020) dEMBF v2.0: an updated database of enzymes for microalgal biofuel feedstock. Plant Cell Physiol 61(5):1019–1024
pubmed: 32061129
Sahoo S, Dehury B, Narang PK, Raina V, Misra N, Suar M (2021) Comprehensive sequence and structure analysis of algal lipid catabolic enzyme Triacylglycerol lipase: an in silico study to vitalize the development of optimum engineered strains with high lipid productivity. J Biomol Struct Dyn 1–19.
Sarma K, Sen P, Barooah M, Choudhury MD, Roychoudhury S, Modi MK (2014) Structural comparison, substrate specificity, and inhibitor binding of AGPase small subunit from monocot and dicot: present insight and future potential. BioMed Res Int 2014:1–4
Sato N, Toyoshima M (2021) Dynamism of Metabolic carbon flow of starch and lipids in Chlamydomonas debaryana. Front Plant Sci 12:501
Schiano di Visconte G, Spicer A, Chuck CJ, Allen MJ (2019) The microalgae biorefinery: a perspective on the current status and future opportunities using genetic modification. Appl Sci 9(22):4793
Schmollinger S, Mühlhaus T, Boyle NR, Blaby IK, Casero D, Mettler T, Merchant SS (2014) Nitrogen-sparing mechanisms in Chlamydomonas affect the transcriptome, the proteome, and photosynthetic metabolism. Plant Cell 26(4):1410–1435
pubmed: 24748044 pmcid: 4036562
Schrödinger L, DeLano W (2020) PyMOL. Retrieved from http://www.pymol.org/pymol
Schulz-Raffelt M, Chochois V, Auroy P, Cuiné S, Billon E, Dauvillée D, Peltier G (2016) Hyper-accumulation of starch and oil in a Chlamydomonas mutant affected in a plant-specific DYRK kinase. Biotechnol Biofuels 9(1):1–12
Seferoglu AB, Koper K, Can FB, Cevahir G, Kavakli IH (2014) Enhanced heterotetrameric assembly of potato ADP-glucose pyrophosphorylase using reverse genetics. Plant Cell Physiol 55(8):1473–1483
pubmed: 24891561
Shokravi Z, Shokravi H, Chyuan OH, Lau WJ, Koloor SSR, Petrů M, Ismail AF (2020) Improving ‘lipid productivity’in microalgae by bilateral enhancement of biomass and lipid contents: a review. Sustainability 12(21):9083
Spassov VZ, Yan L, Flook PK (2007) The dominant role of side-chain backbone interactions in structural realization of amino acid code. ChiRotor: a side-chain prediction algorithm based on side-chain backbone interactions. Protein Sci 16(3):494–506
pubmed: 17242380 pmcid: 2203320
Spassov VZ, Flook PK, Yan L (2008) LOOPER: a molecular mechanics-based algorithm for protein loop prediction. Protein Eng Des Sel 21(2):91–100
pubmed: 18194981
Sun XM, Ren LJ, Zhao QY, Ji XJ, Huang H (2019) Enhancement of lipid accumulation in microalgae by metabolic engineering. Biochimica et Biophysica Acta (BBA) 1864(4):552–566
Sun H, Li J, Song H, Yang D, Deng X, Liu J, Yang M (2020) Comprehensive analysis of AGPase genes uncovers their potential roles in starch biosynthesis in lotus seed. BMC Plant Biol 20(1):1–15
Takahashi K, Ide Y, Hayakawa J, Yoshimitsu Y, Fukuhara I, Abe J, Harayama S (2018) Lipid productivity in TALEN-induced starchless mutants of the unicellular green alga Coccomyxa sp. strain Obi. Algal Res 32:300–307
Tan KWM, Lee YK (2016) The dilemma for lipid productivity in green microalgae: importance of substrate provision in improving oil yield without sacrificing growth. Biotechnol Biofuels 9(1):1–14
Theologis A, Ecker JR, Palm CJ, Federspiel NA, Kaul S, White O, Davis RW (2000) Sequence and analysis of chromosome 1 of the plant Arabidopsis thaliana. Nature 408(6814):816–820
pubmed: 11130712
Trentacoste EM, Shrestha RP, Smith SR, Glé C, Hartmann AC, Hildebrand M, Gerwick WH (2013) Metabolic engineering of lipid catabolism increases microalgal lipid accumulation without compromising growth. Proc Natl Acad Sci 110(49):19748–19753
pubmed: 24248374 pmcid: 3856844
Udayan A, Pandey AK, Sirohi R, Sreekumar N, Sang BI, Sim SJ, Pandey A (2022) Production of microalgae with high lipid content and their potential as sources of nutraceuticals. Phytochem Rev, 1–28.
Vigeolas H, Möhlmann T, Martini N, Neuhaus HE, Geigenberger P (2004) Embryo-specific reduction of ADP-Glc pyrophosphorylase leads to an inhibition of starch synthesis and a delay in oil accumulation in developing seeds of oilseed rape. Plant Physiol 136(1):2676–2686
pubmed: 15333758 pmcid: 523332
Villarreal JV, Burgués C, Rösch C (2020) Acceptability of genetically engineered algae biofuels in Europe: opinions of experts and stakeholders. Biotechnol Biofuels 13(1):1–21
Wang SM, Chu B, Lue WL, Yu TS, Eimert K, Chen J (1997) adg2-1 represents a missense mutation in the ADPG pyrophosphorylase large subunit gene of Arabidopsis thaliana. Plant J 11(5):1121–1126
pubmed: 9193079
Wang SM, Lue WL, Yu TS, Long JH, Wang CN, Eimert K, Chen J (1998) Characterization of ADG1, an Arabidopsis locus encoding for ADPG pyrophosphorylase small subunit, demonstrates that the presence of the small subunit is required for large subunit stability. Plant J 13(1):63–70
pubmed: 9680965
Wang ZT, Ullrich N, Joo S, Waffenschmidt S, Goodenough U (2009) Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. Eukaryot Cell 8(12):1856–1868
pubmed: 19880756 pmcid: 2794211
Weigelt K, Kuster H, Rutten T, Fait A, Fernie AR, Miersch O, Weber H (2009) ADP-glucose pyrophosphorylase-deficient pea embryos reveal specific transcriptional and metabolic changes of carbon-nitrogen metabolism and stress responses. Plant Physiol 149(1):395–411
pubmed: 18987213 pmcid: 2613696
Xu D, Zhang Y (2011) Improving the physical realism and structural accuracy of protein models by a two-step atomic-level energy minimization. Biophys J 101(10):2525–2534
pubmed: 22098752 pmcid: 3218324
Xu X, Vanhercke T, Shrestha P, Luo J, Akbar S, Konik-Rose C, Liu Q (2019) Upregulated lipid biosynthesis at the expense of starch production in potato (Solanum tuberosum) vegetative tissues via simultaneous downregulation of ADP-Glucose Pyrophosphorylase and Sugar Dependent1 expressions. Front Plant Science 10:1444
Yan Y, Tao H, He J, Huang SY (2020) The HDOCK server for integrated protein–protein docking. Nat Protoc 15(5):1829–1852
pubmed: 32269383
Yu L, Fan J, Yan C, Xu C (2018) Starch deficiency enhances lipid biosynthesis and turnover in leaves. Plant Physiol 178(1):118–129
pubmed: 30076222 pmcid: 6130009
Yu L, Fan J, Yan C, Xu C (2018) Starch deficiency enhances lipid biosynthesis and turnover in leaves. Plant Physiol. 178:118–129
pubmed: 30076222 pmcid: 6130009
Zabawinski C, Van Den Koornhuyse N, d’Hulst C, Schlichting R, Giersch C, Delrue B, Ball S (2001) Starchless mutants of Chlamydomonas reinhardtii lack the small subunit of a heterotetrameric ADP-glucose pyrophosphorylase. J Bacteriol 183(3):1069–1077
pubmed: 11208806 pmcid: 94975

Auteurs

Susrita Sahoo (S)

School of Biotechnology, Kalinga Institute of Industrial Technology (KIIT), Deemed to Be University, Bhubaneswar, 751024, India.

Gajraj Singh Khuswaha (GS)

KIIT-Technology Business Incubator (KIIT-TBI), Kalinga Institute of Industrial Technology (KIIT), Deemed to be University, Bhubaneswar, Odisha, 751024, India.
Transcription Regulation Group, International Centre for Genetic Engineering and Biotechnology (ICGEB), New Delhi, 110067, India.

Namrata Misra (N)

School of Biotechnology, Kalinga Institute of Industrial Technology (KIIT), Deemed to Be University, Bhubaneswar, 751024, India. misranamrata8@gmail.com.
KIIT-Technology Business Incubator (KIIT-TBI), Kalinga Institute of Industrial Technology (KIIT), Deemed to be University, Bhubaneswar, Odisha, 751024, India. misranamrata8@gmail.com.

Mrutyunjay Suar (M)

School of Biotechnology, Kalinga Institute of Industrial Technology (KIIT), Deemed to Be University, Bhubaneswar, 751024, India. mrutyunjaysuar80@gmail.com.
KIIT-Technology Business Incubator (KIIT-TBI), Kalinga Institute of Industrial Technology (KIIT), Deemed to be University, Bhubaneswar, Odisha, 751024, India. mrutyunjaysuar80@gmail.com.

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