Nitrogen fixation by diverse diazotrophic communities can support population growth of arboreal ants
Abstract Background Symbiotic ant-plant associations, in which ants live on plants, feed on plant-provided food, and protect host trees against threats, are ubiquitous across the tropics, with the Azteca-Cecropia associations being amongst the most widespread interactions in the Neotropics. Upon col...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-06-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-022-01289-0 |
| _version_ | 1811247917834436608 |
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| author | Maximilian Nepel Josephine Pfeifer Felix B. Oberhauser Andreas Richter Dagmar Woebken Veronika E. Mayer |
| author_facet | Maximilian Nepel Josephine Pfeifer Felix B. Oberhauser Andreas Richter Dagmar Woebken Veronika E. Mayer |
| author_sort | Maximilian Nepel |
| collection | DOAJ |
| description | Abstract Background Symbiotic ant-plant associations, in which ants live on plants, feed on plant-provided food, and protect host trees against threats, are ubiquitous across the tropics, with the Azteca-Cecropia associations being amongst the most widespread interactions in the Neotropics. Upon colonization of Cecropia’s hollow internodes, Azteca queens form small patches with plant parenchyma, which are then used as waste piles when the colony grows. Patches—found in many ant-plant mutualisms—are present throughout the colony life cycle and may supplement larval food. Despite their initial nitrogen (N)-poor substrate, patches in Cecropia accommodate fungi, nematodes, and bacteria. In this study, we investigated the atmospheric N2 fixation as an N source in patches of early and established ant colonies. Results Via 15N2 tracer assays, N2 fixation was frequently detected in all investigated patch types formed by three Azteca ant species. Quantified fixation rates were similar in early and established ant colonies and higher than in various tropical habitats. Based on amplicon sequencing, the identified microbial functional guild—the diazotrophs—harboring and transcribing the dinitrogenase reductase (nifH) gene was highly diverse and heterogeneous across Azteca colonies. The community composition differed between early and established ant colonies and partly between the ant species. Conclusions Our data show that N2 fixation can result in reasonable amounts of N in ant colonies, which might not only enable bacterial, fungal, and nematode growth in the patch ecosystems but according to our calculations can even support the growth of ant populations. The diverse and heterogeneous diazotrophic community implies a functional redundancy, which could provide the ant-plant-patch system with a higher resilience towards changing environmental conditions. Hence, we propose that N2 fixation represents a previously unknown potential to overcome N limitations in arboreal ant colonies. |
| first_indexed | 2024-04-12T15:19:02Z |
| format | Article |
| id | doaj.art-ec7c4cc894d24a7bad901c71b148fcfc |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-12T15:19:02Z |
| publishDate | 2022-06-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-ec7c4cc894d24a7bad901c71b148fcfc2022-12-22T03:27:33ZengBMCBMC Biology1741-70072022-06-0120111310.1186/s12915-022-01289-0Nitrogen fixation by diverse diazotrophic communities can support population growth of arboreal antsMaximilian Nepel0Josephine Pfeifer1Felix B. Oberhauser2Andreas Richter3Dagmar Woebken4Veronika E. Mayer5Department of Botany and Biodiversity Research, University of ViennaDepartment of Microbiology and Ecosystem Science, Centre for Microbiology and Environmental Systems Science, University of ViennaDepartment of Botany and Biodiversity Research, University of ViennaDepartment of Microbiology and Ecosystem Science, Centre for Microbiology and Environmental Systems Science, University of ViennaDepartment of Microbiology and Ecosystem Science, Centre for Microbiology and Environmental Systems Science, University of ViennaDepartment of Botany and Biodiversity Research, University of ViennaAbstract Background Symbiotic ant-plant associations, in which ants live on plants, feed on plant-provided food, and protect host trees against threats, are ubiquitous across the tropics, with the Azteca-Cecropia associations being amongst the most widespread interactions in the Neotropics. Upon colonization of Cecropia’s hollow internodes, Azteca queens form small patches with plant parenchyma, which are then used as waste piles when the colony grows. Patches—found in many ant-plant mutualisms—are present throughout the colony life cycle and may supplement larval food. Despite their initial nitrogen (N)-poor substrate, patches in Cecropia accommodate fungi, nematodes, and bacteria. In this study, we investigated the atmospheric N2 fixation as an N source in patches of early and established ant colonies. Results Via 15N2 tracer assays, N2 fixation was frequently detected in all investigated patch types formed by three Azteca ant species. Quantified fixation rates were similar in early and established ant colonies and higher than in various tropical habitats. Based on amplicon sequencing, the identified microbial functional guild—the diazotrophs—harboring and transcribing the dinitrogenase reductase (nifH) gene was highly diverse and heterogeneous across Azteca colonies. The community composition differed between early and established ant colonies and partly between the ant species. Conclusions Our data show that N2 fixation can result in reasonable amounts of N in ant colonies, which might not only enable bacterial, fungal, and nematode growth in the patch ecosystems but according to our calculations can even support the growth of ant populations. The diverse and heterogeneous diazotrophic community implies a functional redundancy, which could provide the ant-plant-patch system with a higher resilience towards changing environmental conditions. Hence, we propose that N2 fixation represents a previously unknown potential to overcome N limitations in arboreal ant colonies.https://doi.org/10.1186/s12915-022-01289-0Ant-plant interactionAzteca antCecropia plantMicrobial patchDiazotrophy15N2 tracer assay |
| spellingShingle | Maximilian Nepel Josephine Pfeifer Felix B. Oberhauser Andreas Richter Dagmar Woebken Veronika E. Mayer Nitrogen fixation by diverse diazotrophic communities can support population growth of arboreal ants BMC Biology Ant-plant interaction Azteca ant Cecropia plant Microbial patch Diazotrophy 15N2 tracer assay |
| title | Nitrogen fixation by diverse diazotrophic communities can support population growth of arboreal ants |
| title_full | Nitrogen fixation by diverse diazotrophic communities can support population growth of arboreal ants |
| title_fullStr | Nitrogen fixation by diverse diazotrophic communities can support population growth of arboreal ants |
| title_full_unstemmed | Nitrogen fixation by diverse diazotrophic communities can support population growth of arboreal ants |
| title_short | Nitrogen fixation by diverse diazotrophic communities can support population growth of arboreal ants |
| title_sort | nitrogen fixation by diverse diazotrophic communities can support population growth of arboreal ants |
| topic | Ant-plant interaction Azteca ant Cecropia plant Microbial patch Diazotrophy 15N2 tracer assay |
| url | https://doi.org/10.1186/s12915-022-01289-0 |
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