Development of a cell surface display system in Chlamydomonas reinhardtii

Molino, João Vitor Dutra; Carpine, Roberta; Gademann, Karl; Mayfield, Stephen; Sieber, Simon

doi:10.1016/j.algal.2021.102570

Development of a cell surface display system in Chlamydomonas reinhardtii

Journal Article · Fri Dec 03 00:00:00 UTC 2021 · Algal Research

DOI:https://doi.org/10.1016/j.algal.2021.102570· OSTI ID:1853822

Molino, João Vitor Dutra ^[1]; Carpine, Roberta ^[2]; Gademann, Karl ^[2]; Mayfield, Stephen ^[3]; Sieber, Simon ^[2]

Univ. of Zurich (Switzerland); University of California, San Diego
Univ. of Zurich (Switzerland)
Univ. of California, San Diego, CA (United States)

Cell-surface display systems are biotechnological techniques used to express heterologous proteins on the cell surface. Their application depends directly on the cell system used, as well as on the anchoring point for the surface displayed protein. To meet most application demands an inexpensive, safe, and scalable production platform, that reduces the economic barriers for large scale use is needed. Toward this goal, we screened three possible cell surface anchoring points in the green algae Chlamydomonas by fusing mVenus to prospective anchors moieties. The vectors harboring mVenus:anchor were screened for mVenus fluorescence and tested for cellular localization by confocal laser scanning microscopy. This strategy allowed the identification of two functional anchors, one for the cytoplasmic membrane using the MAW8 GPI-anchor signal, and one for the cell wall using the GP1 protein. We also exploited GP1 chemical and biological traits to release the fused proteins efficiently during cell wall shedding. Our work provides a foundation for surface engineering of C reinhardtii supporting both cell biology studies and biotechnology applications.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of California, San Diego, CA (United States)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE), Transportation Office. Bioenergy Technologies Office

Grant/Contract Number:: EE0008246

OSTI ID:: 1853822

Journal Information:: Algal Research, Journal Name: Algal Research Vol. 61; ISSN 2211-9264

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (99)

Microalga-Powered Microswimmers toward Active Cargo Delivery Yasa, Oncay; Erkoc, Pelin; Alapan, Yunus Advanced Materials, Vol. 30, Issue 45 https://doi.org/10.1002/adma.201804130	journal	September 2018
Cell-Surface display of heterologous proteins: From high-throughput screening to environmental applications Chen, Wilfred; Georgiou, George Biotechnology and Bioengineering, Vol. 79, Issue 5 https://doi.org/10.1002/bit.10407	journal	July 2002
Synthesis and assembly of a full-length human monoclonal antibody in algal chloroplasts Tran, Miller; Zhou, Bin; Pettersson, Pär L. Biotechnology and Bioengineering https://doi.org/10.1002/bit.22446	journal	January 2009
Production of recombinant proteins in microalgae at pilot greenhouse scale: Recombinant Protein Production in Algae Gimpel, Javier A.; Hyun, James S.; Schoepp, Nathan G. Biotechnology and Bioengineering, Vol. 112, Issue 2 https://doi.org/10.1002/bit.25357	journal	September 2014
Engineered catalytic biofilms: Site-specific enzyme immobilization onto E. coli curli nanofibers: Catalytic Biofilms Using Engineered Curli Fibers Botyanszki, Zsofia; Tay, Pei Kun R.; Nguyen, Peter Q. Biotechnology and Bioengineering, Vol. 112, Issue 10 https://doi.org/10.1002/bit.25638	journal	May 2015
Antibiotic Algae by Chemical Surface Engineering Kerschgens, Isabel P.; Gademann, Karl ChemBioChem, Vol. 19, Issue 5 https://doi.org/10.1002/cbic.201700553	journal	January 2018
Green Algae as a Drug Delivery System for the Controlled Release of Antibiotics Shchelik, Inga S.; Sieber, Simon; Gademann, Karl Chemistry – A European Journal, Vol. 26, Issue 70 https://doi.org/10.1002/chem.202003821	journal	November 2020
Tipping of flagellar agglutinins by gametes ofChlamydomonas reinhardtii Goodenough, Ursula W. Cell Motility and the Cytoskeleton, Vol. 25, Issue 2 https://doi.org/10.1002/cm.970250207	journal	January 1993
Crystallographic and energetic analysis of binding of selected anions to the yellow variants of green fluorescent protein 1 1Edited by D. C. Rees Wachter, Rebekka M.; Yarbrough, Daniel; Kallio, Karen Journal of Molecular Biology, Vol. 301, Issue 1 https://doi.org/10.1006/jmbi.2000.3905	journal	August 2000
Display of proteins on Bacillus subtilis endospores Kim, Junehyung; Schumann, Wolfgang Cellular and Molecular Life Sciences, Vol. 66, Issue 19 https://doi.org/10.1007/s00018-009-0067-6	journal	June 2009
Display of both N- and C-terminal target fusion proteins on the Aspergillus oryzae cell surface using a chitin-binding module Tabuchi, Soichiro; Ito, Junji; Adachi, Takashi Applied Microbiology and Biotechnology, Vol. 87, Issue 5 https://doi.org/10.1007/s00253-010-2664-6	journal	May 2010
Recent developments in yeast cell surface display toward extended applications in biotechnology Tanaka, Tsutomu; Yamada, Ryosuke; Ogino, Chiaki Applied Microbiology and Biotechnology, Vol. 95, Issue 3 https://doi.org/10.1007/s00253-012-4175-0	journal	June 2012
Bacterial whole-cell biocatalysts by surface display of enzymes: toward industrial application Schüürmann, Jan; Quehl, Paul; Festel, Gunter Applied Microbiology and Biotechnology, Vol. 98, Issue 19 https://doi.org/10.1007/s00253-014-5897-y	journal	August 2014
Yeast arming systems: pros and cons of different protein anchors and other elements required for display Andreu, Cecilia; del Olmo, Marcel lí Applied Microbiology and Biotechnology, Vol. 102, Issue 6 https://doi.org/10.1007/s00253-018-8827-6	journal	February 2018
Strategies to facilitate transgene expression in Chlamydomonas reinhardtii Eichler-Stahlberg, Alke; Weisheit, Wolfram; Ruecker, Ovidiu Planta, Vol. 229, Issue 4 https://doi.org/10.1007/s00425-008-0879-x	journal	January 2009
Insights into the acclimation of Chlamydomonas reinhardtii to sulfur deprivation Pollock, Steve V.; Pootakham, Wirulda; Shibagaki, Nakako Photosynthesis Research, Vol. 86, Issue 3 https://doi.org/10.1007/s11120-005-4048-9	journal	November 2005
Photosynthetic biomanufacturing in green algae; production of recombinant proteins for industrial, nutritional, and medical uses Rasala, Beth A.; Mayfield, Stephen P. Photosynthesis Research, Vol. 123, Issue 3 https://doi.org/10.1007/s11120-014-9994-7	journal	March 2014
Cell Surface Display of Yarrowia lipolytica Lipase Lip2p Using the Cell Wall Protein YlPir1p, Its Characterization, and Application as a Whole-Cell Biocatalyst Yuzbasheva, Evgeniya Y.; Yuzbashev, Tigran V.; Perkovskaya, Natalia I. Applied Biochemistry and Biotechnology, Vol. 175, Issue 8 https://doi.org/10.1007/s12010-015-1557-7	journal	March 2015
Cell surface exposure of the outer membrane protein OmpA of Escherichia coli K-12 Freudl, Roland; MacIntyre, Sheila; Degen, Maria Journal of Molecular Biology, Vol. 188, Issue 3 https://doi.org/10.1016/0022-2836(86)90171-3	journal	April 1986
Suppressor mutations in chlamydomonas reveal a regulatory mechanism for flagellar function Huang, Bessie; Ramanis, Zenta; Luck, David J. L. Cell, Vol. 28, Issue 1 https://doi.org/10.1016/0092-8674(82)90381-6	journal	January 1982
Analysis of a family of ypt genes and their products from Chlamydomonas reinhardtii Dietmaier, Wolfgang; Fabry, Stefan; Huber, Hans Gene, Vol. 158, Issue 1 https://doi.org/10.1016/0378-1119(95)00052-8	journal	January 1995
Nucleotide-metabolizing enzymes in Chlamydomonas flagella. Watanabe, T.; Flavin, M. Journal of Biological Chemistry, Vol. 251, Issue 1 https://doi.org/10.1016/S0021-9258(17)33943-1	journal	January 1976
Cell wall lytic enzyme released by mating gametes of Chlamydomonas reinhardtii is a metalloprotease and digests the sodium perchlorate-insoluble component of cell wall. Matsuda, Y.; Saito, T.; Yamaguchi, T. Journal of Biological Chemistry, Vol. 260, Issue 10 https://doi.org/10.1016/S0021-9258(18)88982-7	journal	May 1985
Developments in the use of baculoviruses for the surface display of complex eukaryotic proteins Grabherr, Reingard; Ernst, Wolfgang; Oker-Blom, Christian Trends in Biotechnology, Vol. 19, Issue 6 https://doi.org/10.1016/S0167-7799(01)01610-9	journal	June 2001
Photosynthetic biomaterials: A pathway towards autotrophic tissue engineering Schenck, Thilo Ludwig; Hopfner, Ursula; Chávez, Myra Noemi Acta Biomaterialia, Vol. 15 https://doi.org/10.1016/j.actbio.2014.12.012	journal	March 2015
Proteases in cancer drug delivery Vandooren, Jennifer; Opdenakker, Ghislain; Loadman, Paul M. Advanced Drug Delivery Reviews, Vol. 97 https://doi.org/10.1016/j.addr.2015.12.020	journal	February 2016
Efficient surface-display of autotransporter proteins in cyanobacteria Ferri, Stefano; Nakamura, Mayumi; Ito, Akiko Algal Research, Vol. 12 https://doi.org/10.1016/j.algal.2015.09.013	journal	November 2015
Nuclear genome shuffling significantly increases production of chloroplast-based recombinant protein in Chlamydomonas reinhardtii Fields, Francis J.; Ostrand, Joseph T.; Tran, Miller Algal Research, Vol. 41 https://doi.org/10.1016/j.algal.2019.101523	journal	August 2019
Recent advancements in the genetic engineering of microalgae Sproles, Ashley E.; Fields, Francis J.; Smalley, Tressa N. Algal Research, Vol. 53 https://doi.org/10.1016/j.algal.2020.102158	journal	March 2021
Development of exosome surface display technology in living human cells Stickney, Zachary; Losacco, Joseph; McDevitt, Sophie Biochemical and Biophysical Research Communications, Vol. 472, Issue 1 https://doi.org/10.1016/j.bbrc.2016.02.058	journal	March 2016
Microneedle-based biosensor for minimally-invasive lactate detection Bollella, Paolo; Sharma, Sanjiv; Cass, Anthony Edward George Biosensors and Bioelectronics, Vol. 123 https://doi.org/10.1016/j.bios.2018.08.010	journal	January 2019
Recovery and purification of plant-made recombinant proteins Wilken, Lisa R.; Nikolov, Zivko L. Biotechnology Advances, Vol. 30, Issue 2 https://doi.org/10.1016/j.biotechadv.2011.07.020	journal	March 2012
Chlamydomonas CAV2 Encodes a Voltage- Dependent Calcium Channel Required for the Flagellar Waveform Conversion Fujiu, Kenta; Nakayama, Yoshitaka; Yanagisawa, Ayaka Current Biology, Vol. 19, Issue 2 https://doi.org/10.1016/j.cub.2008.11.068	journal	January 2009
Using bacteria to express and display anti-parasite molecules in mosquitoes: current and future strategies Riehle, Michael A.; Jacobs-Lorena, Marcelo Insect Biochemistry and Molecular Biology, Vol. 35, Issue 7 https://doi.org/10.1016/j.ibmb.2005.02.008	journal	July 2005
Effects of the microalgae Chlamydomonas on gastrointestinal health Fields, Francis J.; Lejzerowicz, Franck; Schroeder, Dave Journal of Functional Foods, Vol. 65 https://doi.org/10.1016/j.jff.2019.103738	journal	February 2020
Illustrate: Software for Biomolecular Illustration Goodsell, David S.; Autin, Ludovic; Olson, Arthur J. Structure, Vol. 27, Issue 11 https://doi.org/10.1016/j.str.2019.08.011	journal	November 2019
Versatile microbial surface-display for environmental remediation and biofuels production Wu, Cindy H.; Mulchandani, Ashok; Chen, Wilfred Trends in Microbiology, Vol. 16, Issue 4 https://doi.org/10.1016/j.tim.2008.01.003	journal	April 2008
TrackMate: An open and extensible platform for single-particle tracking Tinevez, Jean-Yves; Perry, Nick; Schindelin, Johannes Methods, Vol. 115 https://doi.org/10.1016/j.ymeth.2016.09.016	journal	February 2017
Self-Assembly of Spider Silk-Fusion Proteins Comprising Enzymatic and Fluorescence Activity Humenik, Martin; Mohrand, Madeleine; Scheibel, Thomas Bioconjugate Chemistry, Vol. 29, Issue 4 https://doi.org/10.1021/acs.bioconjchem.7b00759	journal	January 2018
Self-Assembled Multimeric-Enzyme Nanoreactor for Robust and Efficient Biocatalysis Yin, Liang; Guo, Xiang; Liu, Lu ACS Biomaterials Science & Engineering, Vol. 4, Issue 6 https://doi.org/10.1021/acsbiomaterials.8b00279	journal	May 2018
Cyanobacterial Surface Display System Mediates Engineered Interspecies and Abiotic Binding Fedeson, Derek T.; Ducat, Daniel C. ACS Synthetic Biology, Vol. 6, Issue 2 https://doi.org/10.1021/acssynbio.6b00254	journal	November 2016
Birth of a Photosynthetic Chassis: A MoClo Toolkit Enabling Synthetic Biology in the Microalga Chlamydomonas reinhardtii Crozet, Pierre; Navarro, Francisco J.; Willmund, Felix ACS Synthetic Biology, Vol. 7, Issue 9 https://doi.org/10.1021/acssynbio.8b00251	journal	August 2018
Developing a Protein Scaffolding System for Rapid Enzyme Immobilization and Optimization of Enzyme Functions for Biocatalysis Zhang, Guoqiang; Johnston, Timothy; Quin, Maureen B. ACS Synthetic Biology, Vol. 8, Issue 8 https://doi.org/10.1021/acssynbio.9b00187	journal	July 2019
Glycosylated Polyproline II Rods with Kinks as a Structural Motif in Plant Hydroxyproline-Rich Glycoproteins ^† Ferris, Patrick J.; Woessner, Jeffrey P.; Waffenschmidt, Sabine Biochemistry, Vol. 40, Issue 9 https://doi.org/10.1021/bi0023605	journal	March 2001
Engineering Novel and Improved Biocatalysts by Cell Surface Display Smith, Mason R.; Khera, Eshita; Wen, Fei Industrial & Engineering Chemistry Research, Vol. 54, Issue 16 https://doi.org/10.1021/ie504071f	journal	January 2015
Gamete Behaviour in Chlamydomonas Lewin, Ralph A. Nature, Vol. 166, Issue 4210 https://doi.org/10.1038/166076a0	journal	July 1950
Yeast surface display for screening combinatorial polypeptide libraries Boder, Eric T.; Wittrup, K. Dane Nature Biotechnology, Vol. 15, Issue 6 https://doi.org/10.1038/nbt0697-553	journal	June 1997
Surface display of Zymomonas mobilis levansucrase by using the ice-nucleation protein of Pseudomonas syringae Jung, Heung-Chae; Lebeault, Jean-Michel; Pan, Jae-Gu Nature Biotechnology, Vol. 16, Issue 6 https://doi.org/10.1038/nbt0698-576	journal	June 1998
Virus stalls Genzyme plant Bethencourt, Victor Nature Biotechnology, Vol. 27, Issue 8 https://doi.org/10.1038/nbt0809-681a	journal	August 2009
GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization Mori, Toshiyuki; Kuroiwa, Haruko; Higashiyama, Tetsuya Nature Cell Biology, Vol. 8, Issue 1 https://doi.org/10.1038/ncb1345	journal	December 2005
Fiji: an open-source platform for biological-image analysis Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2019	journal	June 2012
Temperature-dependent changes to host–parasite interactions alter the thermal performance of a bacterial host Padfield, Daniel; Castledine, Meaghan; Buckling, Angus The ISME Journal, Vol. 14, Issue 2 https://doi.org/10.1038/s41396-019-0526-5	journal	October 2019
Viral contamination in biologic manufacture and implications for emerging therapies Barone, Paul W.; Wiebe, Michael E.; Leung, James C. Nature Biotechnology, Vol. 38, Issue 5 https://doi.org/10.1038/s41587-020-0507-2	journal	April 2020
Yeast surface display platform for rapid discovery of conformationally selective nanobodies McMahon, Conor; Baier, Alexander S.; Pascolutti, Roberta Nature Structural & Molecular Biology, Vol. 25, Issue 3 https://doi.org/10.1038/s41594-018-0028-6	journal	February 2018
Efficient foreign gene expression in Chlamydomonas reinhardtii mediated by an endogenous intron Lumbreras, Victoria; Stevens, David R.; Purton, Saul The Plant Journal, Vol. 14, Issue 4 https://doi.org/10.1046/j.1365-313X.1998.00145.x	journal	May 1998
Deep-Etch Analysis of Adhesion Complexes Between Gametic Flagellar Membranes of Chlamydomonas Reinhardtii (Chlorophyceae) Goodenough, Ursula W.; Heuser, John E. Journal of Phycology, Vol. 35, Issue 4 https://doi.org/10.1046/j.1529-8817.1999.3540756.x	journal	August 1999
Expression and assembly of a fully active antibody in algae Mayfield, Stephen P.; Franklin, Scott E.; Lerner, Richard A. Proceedings of the National Academy of Sciences, Vol. 100, Issue 2 https://doi.org/10.1073/pnas.0237108100	journal	January 2003
Microoxen: Microorganisms to move microscale loads Weibel, D. B.; Garstecki, P.; Ryan, D. Proceedings of the National Academy of Sciences, Vol. 102, Issue 34 https://doi.org/10.1073/pnas.0505481102	journal	August 2005
Bacterial ratchet motors Di Leonardo, R.; Angelani, L.; Dell'Arciprete, D. Proceedings of the National Academy of Sciences, Vol. 107, Issue 21 https://doi.org/10.1073/pnas.0910426107	journal	May 2010
Production of unique immunotoxin cancer therapeutics in algal chloroplasts Tran, M.; Van, C.; Barrera, D. J. Proceedings of the National Academy of Sciences, Vol. 110, Issue 1 https://doi.org/10.1073/pnas.1214638110	journal	December 2012
Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Gorman, D. S.; Levine, R. P. Proceedings of the National Academy of Sciences, Vol. 54, Issue 6 https://doi.org/10.1073/pnas.54.6.1665	journal	December 1965
Cell wall regeneration in Chlamydomonas: accumulation of mRNAs encoding cell wall hydroxyproline-rich glycoproteins. Adair, W. S.; Apt, K. E. Proceedings of the National Academy of Sciences, Vol. 87, Issue 19 https://doi.org/10.1073/pnas.87.19.7355	journal	October 1990
Identification of Novel Peptidyl Serine α-Galactosyltransferase Gene Family in Plants Saito, Fumie; Suyama, Akiko; Oka, Takuji Journal of Biological Chemistry, Vol. 289, Issue 30 https://doi.org/10.1074/jbc.M114.553933	journal	June 2014
Fluorescence Quantum Yields of Tryptophan and Tyrosine Chen, Raymond F. Analytical Letters, Vol. 1, Issue 1 https://doi.org/10.1080/00032716708051097	journal	January 1967
Micro-nanorobots: important considerations when developing novel drug delivery platforms Singh, Ajay Vikram; Ansari, Mohammad Hasan Dad; Laux, Peter Expert Opinion on Drug Delivery, Vol. 16, Issue 11 https://doi.org/10.1080/17425247.2019.1676228	journal	September 2019
The Chlamydomonas cell wall and its constituent glycoproteins analyzed by the quick-freeze, deep-etch technique Goodenough, U. W. The Journal of Cell Biology, Vol. 101, Issue 4 https://doi.org/10.1083/jcb.101.4.1550	journal	October 1985
Crystals of the Chlamydomonas reinhardtii cell wall: polymerization, depolymerization, and purification of glycoprotein monomers. Goodenough, U. W.; Gebhart, B.; Mecham, R. P. The Journal of Cell Biology, Vol. 103, Issue 2 https://doi.org/10.1083/jcb.103.2.405	journal	August 1986
Nucleated assembly of Chlamydomonas and Volvox cell walls. Adair, W. S.; Steinmetz, S. A.; Mattson, D. M. The Journal of Cell Biology, Vol. 105, Issue 5 https://doi.org/10.1083/jcb.105.5.2373	journal	November 1987
Arabidopsis HAP2/GCS1 is a gamete fusion protein homologous to somatic and viral fusogens Valansi, Clari; Moi, David; Leikina, Evgenia The Journal of Cell Biology, Vol. 216, Issue 3 https://doi.org/10.1083/jcb.201610093	journal	January 2017
Motility occurring in association with the surface of the Chlamydomonas flagellum. Bloodgood, R. A. Journal of Cell Biology, Vol. 75, Issue 3 https://doi.org/10.1083/jcb.75.3.983	journal	December 1977
Yeast-based vaccines: New perspective in vaccine development and application Kumar, Ravinder; Kumar, Piyush FEMS Yeast Research, Vol. 19, Issue 2 https://doi.org/10.1093/femsyr/foz007	journal	January 2019
The Protein Data Bank Berman, H. M. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.235	journal	January 2000
SLiCE: a novel bacterial cell extract-based DNA cloning method Zhang, Yongwei; Werling, Uwe; Edelmann, Winfried Nucleic Acids Research, Vol. 40, Issue 8 https://doi.org/10.1093/nar/gkr1288	journal	January 2012
The Chlamydomonas Hatching Enzyme, Sporangin, is Expressed in Specific Phases of the Cell Cycle and is Localized to the Flagella of Daughter Cells Within the Sporangial Cell Wall Kubo, Takeaki; Kaida, Shinsuke; Abe, Jun Plant and Cell Physiology, Vol. 50, Issue 3 https://doi.org/10.1093/pcp/pcp016	journal	January 2009
Display of β-lactamase on the Escherichia coli surface: outer membrane phenotypes conferred by Lpp′–OmpA′–β-lactamase fusions Georgiou, George; Stephens, Daren L.; Stathopoulos, Christos "Protein Engineering, Design and Selection", Vol. 9, Issue 2 https://doi.org/10.1093/protein/9.2.239	journal	January 1996
A new yeast display vector permitting free scFv amino termini can augment ligand binding affinities Wang, Z.; Mathias, A.; Stavrou, S. Protein Engineering, Design and Selection, Vol. 18, Issue 7 https://doi.org/10.1093/protein/gzi036	journal	June 2005
The conserved plant sterility gene HAP2 functions after attachment of fusogenic membranes in Chlamydomonas and Plasmodium gametes Liu, Y.; Tewari, R.; Ning, J. Genes & Development, Vol. 22, Issue 8 https://doi.org/10.1101/gad.1656508	journal	March 2008
Assembly and Motility of Eukaryotic Cilia and Flagella. Lessons from Chlamydomonas reinhardtii Silflow, Carolyn D.; Lefebvre, Paul A. Plant Physiology, Vol. 127, Issue 4 https://doi.org/10.1104/pp.010807	journal	December 2001
Gene Regulatory Networks for the Haploid-to-Diploid Transition of Chlamydomonas reinhardtii Joo, Sunjoo; Nishimura, Yoshiki; Cronmiller, Evan Plant Physiology, Vol. 175, Issue 1 https://doi.org/10.1104/pp.17.00731	journal	July 2017
The Chlamydomonas reinhardtii Plastid Chromosome : Islands of Genes in a Sea of Repeats Maul, Jude E.; Lilly, Jason W.; Cui, Liying The Plant Cell, Vol. 14, Issue 11 https://doi.org/10.1105/tpc.006155	journal	October 2002
Plus and Minus Sexual Agglutinins from Chlamydomonas reinhardtii Ferris, Patrick J.; Waffenschmidt, Sabine; Umen, James G. The Plant Cell, Vol. 17, Issue 2 https://doi.org/10.1105/tpc.104.028035	journal	February 2005
A Series of Fortunate Events: Introducing Chlamydomonas as a Reference Organism Salomé, Patrice A.; Merchant, Sabeeha S. The Plant Cell, Vol. 31, Issue 8 https://doi.org/10.1105/tpc.18.00952	journal	June 2019
NUTRITIONAL STUDIES WITH CHLAMYDOMONAS REINHARDI Sager, Ruth; Granick, S. Annals of the New York Academy of Sciences, Vol. 56, Issue 5 https://doi.org/10.1111/j.1749-6632.1953.tb30261.x	journal	October 1953
The Chlamydomonas cell cycle Cross, Frederick R.; Umen, James G. The Plant Journal, Vol. 82, Issue 3 https://doi.org/10.1111/tpj.12795	journal	March 2015
Engineered algae: A novel oxygen-generating system for effective treatment of hypoxic cancer Qiao, Yue; Yang, Fei; Xie, Tingting Science Advances, Vol. 6, Issue 21 https://doi.org/10.1126/sciadv.aba5996	journal	May 2020
The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions Merchant, S. S.; Prochnik, S. E.; Vallon, O. Science, Vol. 318, Issue 5848, p. 245-250 https://doi.org/10.1126/science.1143609	journal	October 2007
Production of N -Acetyl- d -Neuraminic Acid by Use of an Efficient Spore Surface Display System Xu, Xiaoman; Gao, Chao; Zhang, Xifeng Applied and Environmental Microbiology, Vol. 77, Issue 10 https://doi.org/10.1128/AEM.00151-11	journal	May 2011
Construction of Yeast Strains with High Cell Surface Lipase Activity by Using Novel Display Systems Based on the Flo1p Flocculation Functional Domain Matsumoto, Takeshi; Fukuda, Hideki; Ueda, Mitsuyoshi Applied and Environmental Microbiology, Vol. 68, Issue 9 https://doi.org/10.1128/AEM.68.9.4517-4522.2002	journal	September 2002
C HLAMYDOMONAS AS A M ODEL O RGANISM Harris, Elizabeth H. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 52, Issue 1 https://doi.org/10.1146/annurev.arplant.52.1.363	journal	June 2001
Molecular organization of cell-wall crystals from Chlamydomonas reinhardtii and Volvox carteri Goodenough, Ursula W.; Heuser, John E. Journal of Cell Science, Vol. 90, Issue 4 https://doi.org/10.1242/jcs.90.4.717	journal	August 1988
Introns mediate post-transcriptional enhancement of nuclear gene expression in the green microalga Chlamydomonas reinhardtii Baier, Thomas; Jacobebbinghaus, Nick; Einhaus, Alexander PLOS Genetics, Vol. 16, Issue 7 https://doi.org/10.1371/journal.pgen.1008944	journal	July 2020
Robust Expression and Secretion of Xylanase1 in Chlamydomonas reinhardtii by Fusion to a Selection Gene and Processing with the FMDV 2A Peptide Rasala, Beth A.; Lee, Philip A.; Shen, Zhouxin PLoS ONE, Vol. 7, Issue 8 https://doi.org/10.1371/journal.pone.0043349	journal	August 2012
Comparison of secretory signal peptides for heterologous protein expression in microalgae: Expanding the secretion portfolio for Chlamydomonas reinhardtii Molino, João Vitor Dutra; de Carvalho, João Carlos Monteiro; Mayfield, Stephen Patrick PLOS ONE, Vol. 13, Issue 2 https://doi.org/10.1371/journal.pone.0192433	journal	February 2018
Some Peculiarities Observed in the Culture of Chlamydomonas Kuwada, Yoshinari Shokubutsugaku Zasshi, Vol. 30, Issue 359 https://doi.org/10.15281/jplantres1887.30.347	journal	January 1916
Mitochondrial Genome Sequence Evolution in Chlamydomonas Popescu, Cristina E.; Lee, Robert W. Genetics, Vol. 175, Issue 2 https://doi.org/10.1534/genetics.106.063156	journal	December 2006
A Decade of Yeast Surface Display Technology: Where Are We Now? Shusta, Eric; Pepper, Lauren; Cho, Yong Combinatorial Chemistry & High Throughput Screening, Vol. 11, Issue 2 https://doi.org/10.2174/138620708783744516	journal	February 2008
Proteases Shape the Chlamydomonas Secretome: Comparison to Classical Neuropeptide Processing Machinery Luxmi, Raj; Blaby-Haas, Crysten; Kumar, Dhivya Proteomes, Vol. 6, Issue 4 https://doi.org/10.3390/proteomes6040036	journal	September 2018
Identification and characterization of EGF receptor in individual exosomes by fluorescence-activated vesicle sorting Higginbotham, James N.; Zhang, Qin; Jeppesen, Dennis K. Journal of Extracellular Vesicles, Vol. 5, Issue 1 https://doi.org/10.3402/jev.v5.29254	journal	January 2016
Green surfing dataset Molino, João Vitor Dutra Zenodo https://doi.org/10.5281/zenodo.4739662	dataset	January 2021

Similar Records

Engineering microalgal cell wall-anchored proteins using GP1 PPSPX motifs and releasing with intein-mediated fusion

Other · Fri Jan 24 04:00:00 UTC 2025 · OSTI ID:2569329

Fixation and stabilization of Escherichia coli cells displaying genetically engineered cell surface proteins

Journal Article · Thu Dec 05 04:00:00 UTC 1996 · Biotechnology and Bioengineering · OSTI ID:398161

Yeast cell surface display for lipase whole cell catalyst and its applications

Journal Article · Fri Aug 01 04:00:00 UTC 2014 · Journal of Molecular Catalysis B: Enzymatic, 106:17-25 · OSTI ID:1170471

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Algae
Cell wall
Chlamydomonas reinhardtii
Cytoplasmic membrane
Perchlorate treatment
Surface display system

Development of a cell surface display system in Chlamydomonas reinhardtii

Citation Formats

References (99)

Similar Records

Related Subjects