Evidence that the domesticated fungus Leucoagaricus gongylophorus recycles its cytoplasmic contents as nutritional rewards to feed its leafcutter ant farmers
Abstract Leafcutter ants farm a fungal cultivar (Leucoagaricus gongylophorus) that converts inedible vegetation into food that sustains colonies with up to millions of workers. Analogous to edible fruits of crops domesticated by humans, L. gongylophorus has evolved specialized nutritional rewards—sw...
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| Format: | Article |
| Language: | English |
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BMC
2023-09-01
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| Series: | IMA Fungus |
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| Online Access: | https://doi.org/10.1186/s43008-023-00126-5 |
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| author | Caio Ambrosio Leal-Dutra Lok Man Yuen Bruno Augusto Maciel Guedes Marta Contreras-Serrano Pedro Elias Marques Jonathan Zvi Shik |
| author_facet | Caio Ambrosio Leal-Dutra Lok Man Yuen Bruno Augusto Maciel Guedes Marta Contreras-Serrano Pedro Elias Marques Jonathan Zvi Shik |
| author_sort | Caio Ambrosio Leal-Dutra |
| collection | DOAJ |
| description | Abstract Leafcutter ants farm a fungal cultivar (Leucoagaricus gongylophorus) that converts inedible vegetation into food that sustains colonies with up to millions of workers. Analogous to edible fruits of crops domesticated by humans, L. gongylophorus has evolved specialized nutritional rewards—swollen hyphal cells called gongylidia that package metabolites and are consumed by ant farmers. Yet, little is known about how gongylidia form, and thus how fungal physiology and ant provisioning collectively govern farming performance. We explored the process of gongylidium formation using advanced microscopy to image the cultivar at scales of nanometers, and both in vitro experiments and in silico analyses to examine the mechanisms of gongylidia formation when isolated from ant farmers. We first used transmission electron, fluorescence, and confocal microscopy imaging to see inside hyphal cells. This imaging showed that the cultivar uses a process called autophagy to recycle its own cellular material (e.g. cytosol, mitochondria) and then shuttles the resulting metabolites into a vacuole whose continual expansion displaces other organelles and causes the gongylidium cell’s bulging bulb-like appearance. We next used scanning electron microscopy and light microscopy to link this intracellular rearrangement to the external branching patterns of gongylidium cells as they clump together into edible bundles called staphyla. We next confirmed that autophagy plays a critical role in gongylidium formation both: (1) in vitro as gongylidium suppression occurred when isolated fungal cultures were grown on media with autophagy inhibitors, and (2) in silico as differential transcript expression (RNA-seq) analyses showed upregulation of multiple autophagy gene isoforms in gongylidia relative to undifferentiated hyphae. While autophagy is a ubiquitous and often highly derived process across the tree of life, our study reveals a new role for autophagy as a mechanism of functional integration between ant farmers and their fungal crop, and potentially as a signifier of higher-level homeostasis between uniquely life-time committed ectosymbionts. |
| first_indexed | 2024-03-09T15:00:38Z |
| format | Article |
| id | doaj.art-05b8fb80fbcf443c9ed42392eacece99 |
| institution | Directory Open Access Journal |
| issn | 2210-6359 |
| language | English |
| last_indexed | 2024-03-09T15:00:38Z |
| publishDate | 2023-09-01 |
| publisher | BMC |
| record_format | Article |
| series | IMA Fungus |
| spelling | doaj.art-05b8fb80fbcf443c9ed42392eacece992023-11-26T13:53:40ZengBMCIMA Fungus2210-63592023-09-0114111310.1186/s43008-023-00126-5Evidence that the domesticated fungus Leucoagaricus gongylophorus recycles its cytoplasmic contents as nutritional rewards to feed its leafcutter ant farmersCaio Ambrosio Leal-Dutra0Lok Man Yuen1Bruno Augusto Maciel Guedes2Marta Contreras-Serrano3Pedro Elias Marques4Jonathan Zvi Shik5Section for Ecology and Evolution, Department of Biology, University of CopenhagenSection for Ecology and Evolution, Department of Biology, University of CopenhagenDepartamento de Ciências Básicas da Vida, Universidade Federal de Juiz de Fora, Campus Governador ValadaresSection for Ecology and Evolution, Department of Biology, University of CopenhagenLaboratory of Molecular Immunology, Department of Microbiology, Immunology and Transplantation, Rega Institute, KU LeuvenSection for Ecology and Evolution, Department of Biology, University of CopenhagenAbstract Leafcutter ants farm a fungal cultivar (Leucoagaricus gongylophorus) that converts inedible vegetation into food that sustains colonies with up to millions of workers. Analogous to edible fruits of crops domesticated by humans, L. gongylophorus has evolved specialized nutritional rewards—swollen hyphal cells called gongylidia that package metabolites and are consumed by ant farmers. Yet, little is known about how gongylidia form, and thus how fungal physiology and ant provisioning collectively govern farming performance. We explored the process of gongylidium formation using advanced microscopy to image the cultivar at scales of nanometers, and both in vitro experiments and in silico analyses to examine the mechanisms of gongylidia formation when isolated from ant farmers. We first used transmission electron, fluorescence, and confocal microscopy imaging to see inside hyphal cells. This imaging showed that the cultivar uses a process called autophagy to recycle its own cellular material (e.g. cytosol, mitochondria) and then shuttles the resulting metabolites into a vacuole whose continual expansion displaces other organelles and causes the gongylidium cell’s bulging bulb-like appearance. We next used scanning electron microscopy and light microscopy to link this intracellular rearrangement to the external branching patterns of gongylidium cells as they clump together into edible bundles called staphyla. We next confirmed that autophagy plays a critical role in gongylidium formation both: (1) in vitro as gongylidium suppression occurred when isolated fungal cultures were grown on media with autophagy inhibitors, and (2) in silico as differential transcript expression (RNA-seq) analyses showed upregulation of multiple autophagy gene isoforms in gongylidia relative to undifferentiated hyphae. While autophagy is a ubiquitous and often highly derived process across the tree of life, our study reveals a new role for autophagy as a mechanism of functional integration between ant farmers and their fungal crop, and potentially as a signifier of higher-level homeostasis between uniquely life-time committed ectosymbionts.https://doi.org/10.1186/s43008-023-00126-5AutophagyLeucoagaricus gongylophorusLeafcutter antGongylidiaFungusSymbiosis |
| spellingShingle | Caio Ambrosio Leal-Dutra Lok Man Yuen Bruno Augusto Maciel Guedes Marta Contreras-Serrano Pedro Elias Marques Jonathan Zvi Shik Evidence that the domesticated fungus Leucoagaricus gongylophorus recycles its cytoplasmic contents as nutritional rewards to feed its leafcutter ant farmers IMA Fungus Autophagy Leucoagaricus gongylophorus Leafcutter ant Gongylidia Fungus Symbiosis |
| title | Evidence that the domesticated fungus Leucoagaricus gongylophorus recycles its cytoplasmic contents as nutritional rewards to feed its leafcutter ant farmers |
| title_full | Evidence that the domesticated fungus Leucoagaricus gongylophorus recycles its cytoplasmic contents as nutritional rewards to feed its leafcutter ant farmers |
| title_fullStr | Evidence that the domesticated fungus Leucoagaricus gongylophorus recycles its cytoplasmic contents as nutritional rewards to feed its leafcutter ant farmers |
| title_full_unstemmed | Evidence that the domesticated fungus Leucoagaricus gongylophorus recycles its cytoplasmic contents as nutritional rewards to feed its leafcutter ant farmers |
| title_short | Evidence that the domesticated fungus Leucoagaricus gongylophorus recycles its cytoplasmic contents as nutritional rewards to feed its leafcutter ant farmers |
| title_sort | evidence that the domesticated fungus leucoagaricus gongylophorus recycles its cytoplasmic contents as nutritional rewards to feed its leafcutter ant farmers |
| topic | Autophagy Leucoagaricus gongylophorus Leafcutter ant Gongylidia Fungus Symbiosis |
| url | https://doi.org/10.1186/s43008-023-00126-5 |
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