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      Algal-fungal symbiosis leads to photosynthetic mycelium

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          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.

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          Yeast, molds and other fungi are found in most environments across the world. Many of the fungi that live on land today form relationships called symbioses with other microbes. Some of these relationships, like those formed with green algae, are beneficial and involve the exchange carbon, nitrogen and other important nutrients. Algae first evolved in the sea and it has been suggested that symbioses with fungi may have helped some algae to leave the water and to colonize the land more than 500 million years ago.

          A fungus called Mortierella elongata grows as a network of filaments in soils and produces large quantities of oils that have various industrial uses. While the details of Mortierella’s life in the wild are still not certain, the fungus is thought to survive by gaining nutrients from decaying matter and it is not known to form any symbioses with algae.

          In 2018, however, a team of researchers reported that, when M. elongata was grown in the laboratory with a marine alga known as Nannochloropsis oceanica, the two organisms appeared to form a symbiosis. Both the alga and fungus produce oil, and when grown together the two organisms produced more oil than when the fungus or algal cells were grown alone. However, it was not clear whether the fungus and alga actually benefit from the symbiosis, for example by exchanging nutrients and helping each other to resist stress.

          Du et al. – including many of the researchers involved in the earlier work – have now used biochemical techniques to study this relationship in more detail. The experiments found that there was a net flow of carbon from algal cells to the fungus, and a net flow of nitrogen in the opposite direction. When nutrients were scarce, algae and fungi grown in the same containers grew better than algae and fungi grown separately. Further, Mortierella only obtained carbon from living algae that attached to the fungal filaments and not from dead algae. Unexpectedly, further experiments found that when grown together over a period of several weeks or more some of the algal cells entered and lived within the filaments of the fungus. Previously, no algae had ever been seen to inhabit the living filaments of a fungus.

          These findings may help researchers to develop improved methods to produce oil from M. elongata and N. oceanica. Furthermore, this partnership provides a convenient new system to study how one organism can live within another and to understand how symbioses between algae and fungi may have first evolved.

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          Most cited references36

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          HUMAN ALTERATION OF THE GLOBAL NITROGEN CYCLE: SOURCES AND CONSEQUENCES

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            A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis.

            The arbuscular mycorrhizal (AM) symbiosis is a mutualistic endosymbiosis formed by plant roots and AM fungi. Most vascular flowering plants have the ability to form these associations, which have a significant impact on plant health and consequently on ecosystem function. Nutrient exchange is a central feature of the AM symbiosis, and AM fungi obtain carbon from their plant host while assisting the plant with the acquisition of phosphorus (as phosphate) from the soil. In the AM symbiosis, the fungus delivers P(i) to the root through specialized hyphae called arbuscules. The molecular mechanisms of P(i) and carbon transfer in the symbiosis are largely unknown, as are the mechanisms by which the plant regulates the symbiosis in response to its nutrient status. Plants possess many classes of P(i) transport proteins, including a unique clade (Pht1, subfamily I), members of which are expressed only in the AM symbiosis. Here, we show that MtPT4, a Medicago truncatula member of subfamily I, is essential for the acquisition of P(i) delivered by the AM fungus. However, more significantly, MtPT4 function is critical for AM symbiosis. Loss of MtPT4 function leads to premature death of the arbuscules; the fungus is unable to proliferate within the root, and symbiosis is terminated. Thus, P(i) transport is not only a benefit for the plant but is also a requirement for the AM symbiosis.
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              Glomalean fungi from the Ordovician.

              Fossilized fungal hyphae and spores from the Ordovician of Wisconsin (with an age of about 460 million years) strongly resemble modern arbuscular mycorrhizal fungi (Glomales, Zygomycetes). These fossils indicate that Glomales-like fungi were present at a time when the land flora most likely only consisted of plants on the bryophytic level. Thus, these fungi may have played a crucial role in facilitating the colonization of land by plants, and the fossils support molecular estimates of fungal phylogeny that place the origin of the major groups of terrestrial fungi (Ascomycota, Basidiomycota, and Glomales) around 600 million years ago.
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                Author and article information

                Contributors
                Role: Senior Editor
                Role: Reviewing Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                16 July 2019
                2019
                : 8
                : e47815
                Affiliations
                [1 ]deptDepartment of Energy-Plant Research Laboratory Michigan State University East LansingUnited States
                [2 ]deptDepartment of Biochemistry and Molecular Biology Michigan State University East LansingUnited States
                [3 ]deptDepartment of Plant Biology Michigan State University East LansingUnited States
                [4 ]deptDepartment of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences Georg-August-University GöttingenGermany
                [5 ]deptCentre of Modern Interdisciplinary Technologies Nicolaus Copernicus University in Toruń ToruńPoland
                [6 ]deptDepartment of Microbiology and Molecular Genetics Michigan State University East LansingUnited States
                [7 ]deptDepartment of Integrative Biology Michigan State University East LansingUnited States
                [8 ]deptDOE Great Lakes Bioenergy Research Center Michigan State University East LansingUnited States
                [9 ]deptDepartment of Plant, Soil and Microbial Sciences Michigan State University East LansingUnited States
                Max Planck Institute for Chemical Ecology Germany
                Boyce Thompson Institute for Plant Research United States
                Boyce Thompson Institute for Plant Research United States
                Boyce Thompson Institute for Plant Research United States
                Università di Torino Italy
                Unversity of Mississippi United States
                Author information
                https://orcid.org/0000-0001-7646-2429
                http://orcid.org/0000-0002-8525-9569
                https://orcid.org/0000-0001-8585-3667
                https://orcid.org/0000-0002-7262-8978
                Article
                47815
                10.7554/eLife.47815
                6634985
                31307571
                392e2f64-fd98-4be7-bbe1-08c4d785aa39
                © 2019, Du et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 19 April 2019
                : 17 June 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000015, U.S. Department of Energy;
                Award ID: DE-FG02-91ER20021
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000015, U.S. Department of Energy;
                Award ID: DE-SC0018409
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000015, U.S. Department of Energy;
                Award ID: DE-FC02-07ER64494
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100011102, European Union Seventh Framework Programme;
                Award ID: FP7/2007-2013 n° [627266]
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DEB 1737898
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Ecology
                Custom metadata
                The capacity for symbiosis between photosynthetic microalgae and early diverging lineages fungi was demonstrated with microscopy and stable isotope exchange of carbon and nitrogen.

                Life sciences
                nannochloropsis oceanica,mortierella elongata,symbiosis,isotope tracers,bioflocculation,other

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