Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata

Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan; Zienkiewicz, Krzysztof; Benning, Nils; Zienkiewicz, Agnieszka; Bonito, Gregory; Benning, Christoph

doi:10.1186/s13068-018-1172-2

Title: Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata

Journal Article · 22 June 2018 · Biotechnology for Biofuels

DOI: https://doi.org/10.1186/s13068-018-1172-2 · OSTI ID:1618724

Du, Zhi-Yan ^[1]; Alvaro, Jonathan ^[2]; Hyden, Brennan ^[3]; Zienkiewicz, Krzysztof ^[4]; Benning, Nils ^[2]; Zienkiewicz, Agnieszka ^[5]; Bonito, Gregory ^[6];

^[7]

Michigan State Univ., East Lansing, MI (United States). Dept. of Energy-Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry and Molecular Biology
Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry and Molecular Biology
Michigan State Univ., East Lansing, MI (United States). Dept. of Energy-Plant Research Lab.
Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry and Molecular Biology; Georg-August-Univ., Goettingen (Germany). Albrecht-von-Haller-Inst. for Plant Sciences, Dept. of Plant Biochemistry
Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry and Molecular Biology; Michigan State Univ., East Lansing, MI (United States). Great Lakes Bioenergy Research Center
Michigan State Univ., East Lansing, MI (United States). Dept. of Plant, Soil and Microbial Sciences; Michigan State Univ., East Lansing, MI (United States). Great Lakes Bioenergy Research Center
Michigan State Univ., East Lansing, MI (United States). Dept. of Energy-Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry and Molecular Biology; Michigan State Univ., East Lansing, MI (United States). Great Lakes Bioenergy Research Center; Michigan State Univ., East Lansing, MI (United States). Dept. of Plant Biology

Background: Although microalgal biofuels have potential advantages over conventional fossil fuels, high production costs limit their application in the market. We developed bio-flocculation and incubation methods for the marine alga, Nannochloropsis oceanica CCMP1779, and the oleaginous fungus, Mortierella elongata AG77, resulting in increased oil productivity. Results: By growing separately and then combining the cells, the M. elongata mycelium could efficiently capture N. oceanica due to an intricate cellular interaction between the two species leading to bio-flocculation. Use of a high-salt culture medium induced accumulation of triacylglycerol (TAG) and enhanced the contents of polyunsaturated fatty acids (PUFAs) including arachidonic acid and docosahexaenoic acid in M. elongata. To increase TAG productivity in the alga, we developed an effective, reduced nitrogen-supply regime based on ammonium in environmental photobioreactors. Under optimized conditions, N. oceanica produced high levels of TAG that could be indirectly monitored by following chlorophyll content. Combining N. oceanica and M. elongata to initiate bio-flocculation yielded high levels of TAG and total fatty acids, with ~ 15 and 22% of total dry weight (DW), respectively, as well as high levels of PUFAs. Genetic engineering of N. oceanica for higher TAG content in nutrient-replete medium was accomplished by overexpressing DGTT5, a gene encoding the type II acyl-CoA:diacylglycerol acyltransferase 5. Combined with bio-flocculation, this approach led to increased production of TAG under nutrient-replete conditions (~ 10% of DW) compared to the wild type (~ 6% of DW). In conclusion, the combined use of M. elongata and N. oceanica with available genomes and genetic engineering tools for both species opens up new avenues to improve biofuel productivity and allows for the engineering of polyunsaturated fatty acids.

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Research Organization:: Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; National Science Foundation (NSF); USDOE

Grant/Contract Number:: SC0018409; FC02-07ER64494; FG02-91ER20021; 627266

OSTI ID:: 1618724

Alternate ID(s):: OSTI ID: 1459413

Journal Information:: Biotechnology for Biofuels, Vol. 11, Issue 1; ISSN 1754-6834

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Transformation of an oleaginous zygomycete Mortierella alpina 1S-4 with the carboxin resistance gene conferred by mutation of the iron–sulfur subunit of succinate dehydrogenase Ando, Akinori; Sakuradani, Eiji; Horinaka, Kota Current Genetics, Vol. 55, Issue 3 https://doi.org/10.1007/s00294-009-0250-1	journal	May 2009
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Triacylglycerol profiling of microalgae Chlamydomonas reinhardtii and Nannochloropsis oceanica Liu, Bensheng; Vieler, Astrid; Li, Chao Bioresource Technology, Vol. 146 https://doi.org/10.1016/j.biortech.2013.07.088	journal	October 2013
Evaluation of the potential of 9 Nannochloropsis strains for biodiesel production Ma, Yubin; Wang, Zhiyao; Yu, Changjiang Bioresource Technology, Vol. 167 https://doi.org/10.1016/j.biortech.2014.06.047	journal	September 2014
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TAG, You’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation Merchant, Sabeeha S.; Kropat, Janette; Liu, Bensheng Current Opinion in Biotechnology, Vol. 23, Issue 3 https://doi.org/10.1016/j.copbio.2011.12.001	journal	June 2012
Data of added-value lipid production, Arachidonic acid, among other lipids by Mortierella elongata , using low cost simulated wastewater Fernandes, Bruna Soares; Fernandes Messias, Márcia Cristina; Carvalho, Patrícia de Oliveira Data in Brief, Vol. 14 https://doi.org/10.1016/j.dib.2017.07.015	journal	October 2017
Producing Designer Oils in Industrial Microalgae by Rational Modulation of Co-evolving Type-2 Diacylglycerol Acyltransferases Xin, Yi; Lu, Yandu; Lee, Yi-Ying Molecular Plant, Vol. 10, Issue 12 https://doi.org/10.1016/j.molp.2017.10.011	journal	December 2017
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Target Cultivation and Financing Parameters for Sustainable Production of Fuel and Feed from Microalgae Gerber, Léda N.; Tester, Jefferson W.; Beal, Colin M. Environmental Science & Technology, Vol. 50, Issue 7 https://doi.org/10.1021/acs.est.5b05381	journal	March 2016
Nontransgenic Marker-Free Gene Disruption by an Episomal CRISPR System in the Oleaginous Microalga, Nannochloropsis oceanica CCMP1779 Poliner, Eric; Takeuchi, Tomomi; Du, Zhi-Yan ACS Synthetic Biology, Vol. 7, Issue 4 https://doi.org/10.1021/acssynbio.7b00362	journal	March 2018
Major fungal lineages are derived from lichen symbiotic ancestors Lutzoni, François; Pagel, Mark; Reeb, Valérie Nature, Vol. 411, Issue 6840 https://doi.org/10.1038/35082053	journal	June 2001
Exploiting diversity and synthetic biology for the production of algal biofuels Georgianna, D. Ryan; Mayfield, Stephen P. Nature, Vol. 488, Issue 7411 https://doi.org/10.1038/nature11479	journal	August 2012
Lipid production in Nannochloropsis gaditana is doubled by decreasing expression of a single transcriptional regulator Ajjawi, Imad; Verruto, John; Aqui, Moena Nature Biotechnology, Vol. 35, Issue 7 https://doi.org/10.1038/nbt.3865	journal	June 2017
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Cell surface characteristics of Mortierella species and their interaction with a mycoparasite Manocha, M. S. Canadian Journal of Microbiology, Vol. 30, Issue 3 https://doi.org/10.1139/m84-044	journal	March 1984
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Fungal-assisted algal flocculation: application in wastewater treatment and biofuel production Muradov, Nazim; Taha, Mohamed; Miranda, Ana F. Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0210-6	journal	January 2015
Lipid production in association of filamentous fungi with genetically modified cyanobacterial cells Miranda, Ana F.; Taha, Mohamed; Wrede, Digby Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0364-2	journal	November 2015
Mycoalgae biofilm: development of a novel platform technology using algae and fungal cultures Rajendran, Aravindan; Hu, Bo Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0533-y	journal	May 2016
Applications of microalgal biofilms for wastewater treatment and bioenergy production Miranda, Ana F.; Ramkumar, Narasimhan; Andriotis, Constandino Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0798-9	journal	May 2017
Transformation of oil-producing fungus, Mortierella alpina 1S-4, using Zeocin, and application to arachidonic acid production Takeno, Seiki; Sakuradani, Eiji; Tomi, Akiko Journal of Bioscience and Bioengineering, Vol. 100, Issue 6 https://doi.org/10.1263/jbb.100.617	journal	December 2005
Genome, Functional Gene Annotation, and Nuclear Transformation of the Heterokont Oleaginous Alga Nannochloropsis oceanica CCMP1779 Vieler, Astrid; Wu, Guangxi; Tsai, Chia-Hong PLoS Genetics, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pgen.1003064	journal	November 2012
Nannochloropsis Genomes Reveal Evolution of Microalgal Oleaginous Traits Wang, Dongmei; Ning, Kang; Li, Jing PLoS Genetics, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pgen.1004094	journal	January 2014
Genome Characterization of the Oleaginous Fungus Mortierella alpina Wang, Lei; Chen, Wei; Feng, Yun PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0028319	journal	December 2011
Engineering challenges in biodiesel production from microalgae Aguirre, Ana-Maria; Bassi, Amarjeet; Saxena, Priyanka Critical Reviews in Biotechnology, Vol. 33, Issue 3 https://doi.org/10.3109/07388551.2012.695333	journal	June 2012
Review of Microalgae Harvesting via Co-Pelletization with Filamentous Fungus Gultom, Sarman; Hu, Bo Energies, Vol. 6, Issue 11 https://doi.org/10.3390/en6115921	journal	November 2013
Lipid Production from Nannochloropsis Ma, Xiao-Nian; Chen, Tian-Peng; Yang, Bo Marine Drugs, Vol. 14, Issue 4 https://doi.org/10.3390/md14040061	journal	March 2016

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Algal-fungal symbiosis leads to photosynthetic mycelium Du, Zhi-Yan; Zienkiewicz, Krzysztof; Vande Pol, Natalie eLife, Vol. 8 https://doi.org/10.7554/elife.47815	journal	July 2019
Algae and fungi move from the past to the future Bonfante, Paola eLife, Vol. 8 https://doi.org/10.7554/elife.49448	journal	July 2019
Algal-fungal symbiosis leads to photosynthetic mycelium Du, Zhi-Yan; Zienkiewicz, Krzysztof; Vande Pol, Natalie eLife, Vol. 8 https://doi.org/10.7554/elife.47815	journal	July 2019
Algae and fungi move from the past to the future Bonfante, Paola eLife, Vol. 8 https://doi.org/10.7554/elife.49448	journal	July 2019

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Related Subjects

09 BIOMASS FUELS
Nannochloropsis
Mortierella
Bio‑flocculation
Polyunsaturated fatty acid
Triacylglycerol
Photobioreactor
Microalgae
Filamentous fungi
Cell–wall interaction
Biofuel
Nitrogen starvation

Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.1186/s13068-018-1172-2 The current record is supplemented by this journal	journal	June 2018
MOESM1 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651188 The current record is supplemented by this dataset	dataset	June 2018
MOESM1 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651188.v1 The current record is supplemented by this figure	figure	June 2018
MOESM2 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651215 The current record is supplemented by this figure	figure	June 2018
MOESM2 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651215.v1 The current record is supplemented by this figure	figure	June 2018
MOESM3 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Dan, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651233 The current record is supplemented by this dataset	dataset	June 2018
MOESM3 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651233.v1 The current record is supplemented by this dataset	dataset	June 2018
MOESM4 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651251 The current record is supplemented by this figure	figure	June 2018
MOESM4 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651251.v1 The current record is supplemented by this dataset	dataset	June 2018
MOESM5 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651269 The current record is supplemented by this dataset	dataset	June 2018
MOESM5 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651269.v1 The current record is supplemented by this dataset	dataset	June 2018
MOESM6 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651281 The current record is supplemented by this figure	figure	June 2018
MOESM6 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651281.v1 The current record is supplemented by this dataset	dataset	June 2018
MOESM7 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651296 The current record is supplemented by this figure	figure	June 2018
MOESM7 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651296.v1 The current record is supplemented by this dataset	dataset	June 2018
MOESM8 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651314 The current record is supplemented by this dataset	dataset	June 2018
MOESM8 of Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.6651314.v1 The current record is supplemented by this figure	figure	June 2018
Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.c.4142111 The current record is supplemented by this dataset	dataset	June 2018
Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata [Supplemental Data] Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan https://doi.org/10.6084/m9.figshare.c.4142111.v1 The current record is supplemented by this figure	figure	June 2018