Algal-fungal symbiosis leads to photosynthetic mycelium
Abstract
Mutualistic interactions between free-living algae and fungi are widespread in nature and are hypothesized to have facilitated the evolution of land plants and lichens. In all known algal-fungal mutualisms, including lichens, algal cells remain external to fungal cells. Here, we report on an algal–fungal interaction in which Nannochloropsis oceanica algal cells become internalized within the hyphae of the fungus Mortierella elongata. This apparent symbiosis begins with close physical contact and nutrient exchange, including carbon and nitrogen transfer between fungal and algal cells as demonstrated by isotope tracer experiments. This mutualism appears to be stable, as both partners remain physiologically active over months of co-cultivation, leading to the eventual internalization of photosynthetic algal cells, which persist to function, grow and divide within fungal hyphae. Nannochloropsis and Mortierella are biotechnologically important species for lipids and biofuel production, with available genomes and molecular tool kits. Based on the current observations, they provide unique opportunities for studying fungal-algal mutualisms including mechanisms leading to endosymbiosis.
- Authors:
-
[1];
[2];
[5];
[6]
- Department of Energy-Plant Research Laboratory, Michigan State University, East Lansing, United States, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States, Department of Plant Biology, Michigan State University, East Lansing, United States
- Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States, Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, Georg-August-University, Göttingen, Germany, Centre of Modern Interdisciplinary Technologies, Nicolaus Copernicus University in Toruń, Toruń, Poland
- Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, United States
- Department of Integrative Biology, Michigan State University, East Lansing, United States, DOE Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, United States
- Department of Energy-Plant Research Laboratory, Michigan State University, East Lansing, United States, DOE Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, United States, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States, Department of Plant Biology, Michigan State University, East Lansing, United States
- Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, United States, DOE Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, United States, Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, United States
- Publication Date:
- Research Org.:
- Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1542666
- Alternate Identifier(s):
- OSTI ID: 1542667; OSTI ID: 1607874
- Grant/Contract Number:
- FG02-91ER20021; SC0018409; FC02-07ER64494
- Resource Type:
- Published Article
- Journal Name:
- eLife
- Additional Journal Information:
- Journal Name: eLife Journal Volume: 8; Journal ID: ISSN 2050-084X
- Publisher:
- eLife Sciences Publications, Ltd.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Du, Zhi-Yan, Zienkiewicz, Krzysztof, Vande Pol, Natalie, Ostrom, Nathaniel E., Benning, Christoph, and Bonito, Gregory M. Algal-fungal symbiosis leads to photosynthetic mycelium. United States: N. p., 2019.
Web. doi:10.7554/eLife.47815.
Du, Zhi-Yan, Zienkiewicz, Krzysztof, Vande Pol, Natalie, Ostrom, Nathaniel E., Benning, Christoph, & Bonito, Gregory M. Algal-fungal symbiosis leads to photosynthetic mycelium. United States. https://doi.org/10.7554/eLife.47815
Du, Zhi-Yan, Zienkiewicz, Krzysztof, Vande Pol, Natalie, Ostrom, Nathaniel E., Benning, Christoph, and Bonito, Gregory M. Tue .
"Algal-fungal symbiosis leads to photosynthetic mycelium". United States. https://doi.org/10.7554/eLife.47815.
@article{osti_1542666,
title = {Algal-fungal symbiosis leads to photosynthetic mycelium},
author = {Du, Zhi-Yan and Zienkiewicz, Krzysztof and Vande Pol, Natalie and Ostrom, Nathaniel E. and Benning, Christoph and Bonito, Gregory M.},
abstractNote = {Mutualistic interactions between free-living algae and fungi are widespread in nature and are hypothesized to have facilitated the evolution of land plants and lichens. In all known algal-fungal mutualisms, including lichens, algal cells remain external to fungal cells. Here, we report on an algal–fungal interaction in which Nannochloropsis oceanica algal cells become internalized within the hyphae of the fungus Mortierella elongata. This apparent symbiosis begins with close physical contact and nutrient exchange, including carbon and nitrogen transfer between fungal and algal cells as demonstrated by isotope tracer experiments. This mutualism appears to be stable, as both partners remain physiologically active over months of co-cultivation, leading to the eventual internalization of photosynthetic algal cells, which persist to function, grow and divide within fungal hyphae. Nannochloropsis and Mortierella are biotechnologically important species for lipids and biofuel production, with available genomes and molecular tool kits. Based on the current observations, they provide unique opportunities for studying fungal-algal mutualisms including mechanisms leading to endosymbiosis.},
doi = {10.7554/eLife.47815},
journal = {eLife},
number = ,
volume = 8,
place = {United States},
year = {2019},
month = {7}
}
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Works referenced in this record:
Coupled N, C and S stable isotope measurements using a dual-column gas chromatography system
journal, January 2007
- Fry, Brian
- Rapid Communications in Mass Spectrometry, Vol. 21, Issue 5
Evidence for a facultative mutualist nutritional relationship between the green coccoid alga Bracteacoccus sp. (Chlorophyceae) and the zoosporic fungus Rhizidium phycophilum (Chytridiomycota)
journal, May 2013
- Picard, Kathryn T.; Letcher, Peter M.; Powell, Martha J.
- Fungal Biology, Vol. 117, Issue 5
Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis
journal, November 2013
- Tisserant, E.; Malbreil, M.; Kuo, A.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 50
Characterization of theGeosiphon pyriforme symbiosome by affinity techniques: confocal laser scanning microscopy (CLSM) and electron microscopy
journal, March 1996
- Sch��ler, A.; Bonfante, P.; Schnepf, E.
- Protoplasma, Vol. 190, Issue 1-2
Nutritional Aspects of Mortierella hygrophila Linn.
journal, April 1956
- Thornton, R. H.
- Nature, Vol. 177, Issue 4510
From Lamarckian fertilizers to fungal castles: recapturing the pre-1985 literature on endophytic and saprotrophic fungi associated with ectomycorrhizal root systems
journal, January 2005
- Summerbell, Richard C.
- Studies in Mycology, Vol. 53
Diversity Patterns, Ecology and Biological Activities of Fungal Communities Associated with the Endemic Macroalgae Across the Antarctic Peninsula
journal, February 2014
- Furbino, Laura E.; Godinho, Valéria M.; Santiago, Iara F.
- Microbial Ecology, Vol. 67, Issue 4
Niche engineering demonstrates a latent capacity for fungal-algal mutualism
journal, July 2014
- Hom, Erik F. Y.; Murray, Andrew W.
- Science, Vol. 345, Issue 6192
CONDITIONAL PRODUCTION OF A FUNCTIONAL FISH GROWTH HORMONE IN THE TRANSGENIC LINE OF NANNOCHLOROPSIS OCULATA (EUSTIGMATOPHYCEAE)
journal, June 2008
- Chen, Hsin Liang; Li, Si Shen; Huang, Rang
- Journal of Phycology, Vol. 44, Issue 3
Flexibility in Algal Endosymbioses Shapes Growth in Reef Corals
journal, June 2004
- Little, A. F.
- Science, Vol. 304, Issue 5676
Glomalean Fungi from the Ordovician
journal, September 2000
- Redecker, D.
- Science, Vol. 289, Issue 5486
Galactoglycerolipid Lipase PGD1 Is Involved in Thylakoid Membrane Remodeling in Response to Adverse Environmental Conditions in Chlamydomonas
journal, February 2018
- Du, Zhi-Yan; Lucker, Ben Franklin; Zienkiewicz, Krzysztof
- The Plant Cell
Contemporaneous radiations of fungi and plants linked to symbiosis
journal, December 2018
- Lutzoni, François; Nowak, Michael D.; Alfaro, Michael E.
- Nature Communications, Vol. 9, Issue 1
Human Alteration of the Global Nitrogen Cycle: Sources and Consequences
journal, August 1997
- Vitousek, Peter M.; Aber, John D.; Howarth, Robert W.
- Ecological Applications, Vol. 7, Issue 3
A Gene Cluster Encoding Rhizoxin Biosynthesis in “Burkholderia rhizoxina”, the Bacterial Endosymbiont of the FungusRhizopus microsporus
journal, January 2007
- Partida-Martinez, Laila P.; Hertweck, Christian
- ChemBioChem, Vol. 8, Issue 1
Engineering microbial consortia: a new frontier in synthetic biology
journal, September 2008
- Brenner, Katie; You, Lingchong; Arnold, Frances H.
- Trends in Biotechnology, Vol. 26, Issue 9, p. 483-489
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens
journal, February 2017
- Uehling, J.; Gryganskyi, A.; Hameed, K.
- Environmental Microbiology, Vol. 19, Issue 8
Chemodenitrification in the cryoecosystem of Lake Vida, Victoria Valley, Antarctica
journal, July 2016
- Ostrom, N. E.; Gandhi, H.; Trubl, G.
- Geobiology, Vol. 14, Issue 6
A Galactoglycerolipid Lipase Is Required for Triacylglycerol Accumulation and Survival Following Nitrogen Deprivation in Chlamydomonas reinhardtii
journal, November 2012
- Li, Xiaobo; Moellering, Eric R.; Liu, Bensheng
- The Plant Cell, Vol. 24, Issue 11
Genome, Functional Gene Annotation, and Nuclear Transformation of the Heterokont Oleaginous Alga Nannochloropsis oceanica CCMP1779
journal, November 2012
- Vieler, Astrid; Wu, Guangxi; Tsai, Chia-Hong
- PLoS Genetics, Vol. 8, Issue 11
A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis
journal, January 2007
- Javot, H.; Penmetsa, R. V.; Terzaghi, N.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 5
Stress-induced neutral lipid biosynthesis in microalgae — Molecular, cellular and physiological insights
journal, September 2016
- Zienkiewicz, Krzysztof; Du, Zhi-Yan; Ma, Wei
- Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1861, Issue 9
Basidiomycete yeasts in the cortex of ascomycete macrolichens
journal, July 2016
- Spribille, Toby; Tuovinen, Veera; Resl, Philipp
- Science, Vol. 353, Issue 6298
Hyphal Growth: a Tale of Motors, Lipids, and the Spitzenkörper
journal, January 2007
- Steinberg, Gero
- Eukaryotic Cell, Vol. 6, Issue 3
Ectomycorrhizal fungi contribute to soil organic matter cycling in sub-boreal forests
journal, October 2013
- Phillips, Lori A.; Ward, Valerie; Jones, Melanie D.
- The ISME Journal, Vol. 8, Issue 3
A simple procedure for dissolving fungal cell wall preparations for the analysis of neutral sugars
journal, September 1992
- Velichkov, A. D.
- World Journal of Microbiology & Biotechnology, Vol. 8, Issue 5
A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data
journal, September 2016
- Spatafora, Joseph W.; Chang, Ying; Benny, Gerald L.
- Mycologia, Vol. 108, Issue 5
Vertical Transmission of Endobacteria in the Arbuscular Mycorrhizal Fungus Gigaspora margarita through Generation of Vegetative Spores
journal, June 2004
- Bianciotto, V.; Genre, A.; Jargeat, P.
- Applied and Environmental Microbiology, Vol. 70, Issue 6
Expression of a symbiosis-specific gene in Symbiodinium type A1 associated with coral, nudibranch and giant clam larvae
journal, May 2017
- Mies, M.; Voolstra, C. R.; Castro, C. B.
- Royal Society Open Science, Vol. 4, Issue 5
A Source of Terrestrial Organic Carbon to Investigate the Browning of Aquatic Ecosystems
journal, October 2013
- Lennon, Jay T.; Hamilton, Stephen K.; Muscarella, Mario E.
- PLoS ONE, Vol. 8, Issue 10
Self-supporting artificial system of the green alga Chlamydomonas reinhardtii and the ascomycetous fungus Alternaria infectoria
journal, June 2016
- Simon, Janka; Kósa, Annamária; Bóka, Károly
- Symbiosis, Vol. 71, Issue 3
The protein Compromised Hydrolysis of Triacylglycerols 7 (CHT7) acts as a repressor of cellular quiescence in Chlamydomonas
journal, October 2014
- Tsai, C. -H.; Warakanont, J.; Takeuchi, T.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 44
Isolating a functionally relevant guild of fungi from the root microbiome of Populus
journal, August 2016
- Bonito, Gregory; Hameed, Khalid; Ventura, Rafael
- Fungal Ecology, Vol. 22
Algal ancestor of land plants was preadapted for symbiosis
journal, October 2015
- Delaux, Pierre-Marc; Radhakrishnan, Guru V.; Jayaraman, Dhileepkumar
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 43
Ultrastructure and Composition of the Nannochloropsis gaditana Cell Wall
journal, September 2014
- Scholz, Matthew J.; Weiss, Taylor L.; Jinkerson, Robert E.
- Eukaryotic Cell, Vol. 13, Issue 11
Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata
journal, June 2018
- Du, Zhi-Yan; Alvaro, Jonathan; Hyden, Brennan
- Biotechnology for Biofuels, Vol. 11, Issue 1
Fungal communities of lichen-dominated biological soil crusts: Diversity, relative microbial biomass, and their relationship to disturbance and crust cover
journal, October 2010
- Bates, Scott T.; Nash, Thomas H.; Sweat, Ken G.
- Journal of Arid Environments, Vol. 74, Issue 10
Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils
journal, September 2013
- Brown, Shawn P.; Jumpponen, Ari
- Molecular Ecology, Vol. 23, Issue 2
Functional analysis of liverworts in dual symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated Palaeozoic CO2 decline
journal, November 2015
- Field, Katie J.; Rimington, William R.; Bidartondo, Martin I.
- The ISME Journal, Vol. 10, Issue 6
Studies on initiation and development of the partner association inGeosiphon pyriforme (K�tz.) v. Wettstein, a unique endocytobiotic system of a fungus (Glomales) and the cyanobacteriumNostoc punctiforme (K�tz.) Hariot
journal, March 1996
- Mollenhauer, D.; Mollenhauer, R.; Kluge, M.
- Protoplasma, Vol. 193, Issue 1-4
Works referencing / citing this record: