Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities
Abstract Background The root mycobiome plays a fundamental role in plant nutrition and protection against biotic and abiotic stresses. In temperate forests or meadows dominated by angiosperms, the numerous fungi involved in root symbioses are often shared between neighboring plants, thus forming com...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2022-07-01
|
| Series: | Environmental Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40793-022-00434-0 |
| _version_ | 1828260231944077312 |
|---|---|
| author | Benoît Perez-Lamarque Rémi Petrolli Christine Strullu-Derrien Dominique Strasberg Hélène Morlon Marc-André Selosse Florent Martos |
| author_facet | Benoît Perez-Lamarque Rémi Petrolli Christine Strullu-Derrien Dominique Strasberg Hélène Morlon Marc-André Selosse Florent Martos |
| author_sort | Benoît Perez-Lamarque |
| collection | DOAJ |
| description | Abstract Background The root mycobiome plays a fundamental role in plant nutrition and protection against biotic and abiotic stresses. In temperate forests or meadows dominated by angiosperms, the numerous fungi involved in root symbioses are often shared between neighboring plants, thus forming complex plant-fungus interaction networks of weak specialization. Whether this weak specialization also holds in rich tropical communities with more phylogenetically diverse sets of plant lineages remains unknown. We collected roots of 30 plant species in semi-natural tropical communities including angiosperms, ferns, and lycophytes, in three different habitat types on La Réunion island: a recent lava flow, a wet thicket, and an ericoid shrubland. We identified root-inhabiting fungi by sequencing both the 18S rRNA and the ITS2 variable regions. We assessed the diversity of mycorrhizal fungal taxa according to plant species and lineages, as well as the structure and specialization of the resulting plant-fungus networks. Results The 18S and ITS2 datasets are highly complementary at revealing the root mycobiota. According to 18S, Glomeromycotina colonize all plant groups in all habitats forming the least specialized interactions, resulting in nested network structures, while Mucoromycotina (Endogonales) are more abundant in the wetland and show higher specialization and modularity compared to the former. According to ITS2, mycorrhizal fungi of Ericaceae and Orchidaceae, namely Helotiales, Sebacinales, and Cantharellales, also colonize the roots of most plant lineages, confirming that they are frequent endophytes. While Helotiales and Sebacinales present intermediate levels of specialization, Cantharellales are more specialized and more sporadic in their interactions with plants, resulting in highly modular networks. Conclusions This study of the root mycobiome in tropical environments reinforces the idea that mycorrhizal fungal taxa are locally shared between co-occurring plants, including phylogenetically distant plants (e.g. lycophytes and angiosperms), where they may form functional mycorrhizae or establish endophytic colonization. Yet, we demonstrate that, irrespectively of the environmental variations, the level of specialization significantly varies according to the fungal lineages, probably reflecting the different evolutionary origins of these plant-fungus symbioses. Frequent fungal sharing between plants questions the roles of the different fungi in community functioning and highlights the importance of considering networks of interactions rather than isolated hosts. |
| first_indexed | 2024-04-13T03:21:04Z |
| format | Article |
| id | doaj.art-3acc252196554c77a14086ef1044c815 |
| institution | Directory Open Access Journal |
| issn | 2524-6372 |
| language | English |
| last_indexed | 2024-04-13T03:21:04Z |
| publishDate | 2022-07-01 |
| publisher | BMC |
| record_format | Article |
| series | Environmental Microbiome |
| spelling | doaj.art-3acc252196554c77a14086ef1044c8152022-12-22T03:04:47ZengBMCEnvironmental Microbiome2524-63722022-07-0117111910.1186/s40793-022-00434-0Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communitiesBenoît Perez-Lamarque0Rémi Petrolli1Christine Strullu-Derrien2Dominique Strasberg3Hélène Morlon4Marc-André Selosse5Florent Martos6Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, UAInstitut de Systématique, Évolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, UAInstitut de Systématique, Évolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, UAPeuplements Végétaux et Bioagresseurs en Milieu Tropical, UMR PVBMT, Université de La RéunionInstitut de Biologie de l’École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, Université PSLInstitut de Systématique, Évolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, UAInstitut de Systématique, Évolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, UAAbstract Background The root mycobiome plays a fundamental role in plant nutrition and protection against biotic and abiotic stresses. In temperate forests or meadows dominated by angiosperms, the numerous fungi involved in root symbioses are often shared between neighboring plants, thus forming complex plant-fungus interaction networks of weak specialization. Whether this weak specialization also holds in rich tropical communities with more phylogenetically diverse sets of plant lineages remains unknown. We collected roots of 30 plant species in semi-natural tropical communities including angiosperms, ferns, and lycophytes, in three different habitat types on La Réunion island: a recent lava flow, a wet thicket, and an ericoid shrubland. We identified root-inhabiting fungi by sequencing both the 18S rRNA and the ITS2 variable regions. We assessed the diversity of mycorrhizal fungal taxa according to plant species and lineages, as well as the structure and specialization of the resulting plant-fungus networks. Results The 18S and ITS2 datasets are highly complementary at revealing the root mycobiota. According to 18S, Glomeromycotina colonize all plant groups in all habitats forming the least specialized interactions, resulting in nested network structures, while Mucoromycotina (Endogonales) are more abundant in the wetland and show higher specialization and modularity compared to the former. According to ITS2, mycorrhizal fungi of Ericaceae and Orchidaceae, namely Helotiales, Sebacinales, and Cantharellales, also colonize the roots of most plant lineages, confirming that they are frequent endophytes. While Helotiales and Sebacinales present intermediate levels of specialization, Cantharellales are more specialized and more sporadic in their interactions with plants, resulting in highly modular networks. Conclusions This study of the root mycobiome in tropical environments reinforces the idea that mycorrhizal fungal taxa are locally shared between co-occurring plants, including phylogenetically distant plants (e.g. lycophytes and angiosperms), where they may form functional mycorrhizae or establish endophytic colonization. Yet, we demonstrate that, irrespectively of the environmental variations, the level of specialization significantly varies according to the fungal lineages, probably reflecting the different evolutionary origins of these plant-fungus symbioses. Frequent fungal sharing between plants questions the roles of the different fungi in community functioning and highlights the importance of considering networks of interactions rather than isolated hosts.https://doi.org/10.1186/s40793-022-00434-0Common mycorrhizal networksEndomycorrhizaRoot endophytismMucoromycotina fine root endophytesEarly-diverging plantsFungal metabarcoding |
| spellingShingle | Benoît Perez-Lamarque Rémi Petrolli Christine Strullu-Derrien Dominique Strasberg Hélène Morlon Marc-André Selosse Florent Martos Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities Environmental Microbiome Common mycorrhizal networks Endomycorrhiza Root endophytism Mucoromycotina fine root endophytes Early-diverging plants Fungal metabarcoding |
| title | Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities |
| title_full | Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities |
| title_fullStr | Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities |
| title_full_unstemmed | Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities |
| title_short | Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities |
| title_sort | structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities |
| topic | Common mycorrhizal networks Endomycorrhiza Root endophytism Mucoromycotina fine root endophytes Early-diverging plants Fungal metabarcoding |
| url | https://doi.org/10.1186/s40793-022-00434-0 |
| work_keys_str_mv | AT benoitperezlamarque structureandspecializationofmycorrhizalnetworksinphylogeneticallydiversetropicalcommunities AT remipetrolli structureandspecializationofmycorrhizalnetworksinphylogeneticallydiversetropicalcommunities AT christinestrulluderrien structureandspecializationofmycorrhizalnetworksinphylogeneticallydiversetropicalcommunities AT dominiquestrasberg structureandspecializationofmycorrhizalnetworksinphylogeneticallydiversetropicalcommunities AT helenemorlon structureandspecializationofmycorrhizalnetworksinphylogeneticallydiversetropicalcommunities AT marcandreselosse structureandspecializationofmycorrhizalnetworksinphylogeneticallydiversetropicalcommunities AT florentmartos structureandspecializationofmycorrhizalnetworksinphylogeneticallydiversetropicalcommunities |