Context-dependent and variable effects of endohyphal bacteria on interactions between fungi and seeds

Authors: SHAFFER, JUSTIN - University Of Arizona; ZALAMEA, PAUL - Smithsonian Tropical Research; SARMIENTO, C - Smithsonian Tropical Research; GALLERY, RACHEL - University Of Arizona; DALLING, JAMES - University Of Illinois; Davis, Adam; BALTRUS, DAVID - University Of Arizona; ARNOLD, A - University Of Arizona

Submitted to: Fungal Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/21/2018
Publication Date: 10/10/2018
Citation: Shaffer, J.P., Zalamea, P.C., Sarmiento, C., Gallery, R.E., Dalling, J.W., Davis, A.S., Baltrus, D.A., Arnold, A.E. 2018. Context-dependent and variable effects of endohyphal bacteria on interactions between fungi and seeds. Fungal Ecology. 36:117-127. https://doi.org/10.1016/j.funeco.2018.08.008.
DOI: https://doi.org/10.1016/j.funeco.2018.08.008

Interpretive Summary: Pioneer plant species, such as agricultural weeds and pioneer trees of tropical forests, are early colonizers of disturbed soils. Improved understanding of factors that affect the longevity of seeds in soils can have practical implications, including better ways of depleting weed seedbanks in agricultural systems or conserving tree species in tropical forests. Soil fungi are one of the main sources of seed demise in soils. Fungal effects on plants can be influenced by the presence of endohyphal bacteria, which live within fungal hyphae and can alter the way fungi function. Here, we conducted the first experiments to date that quantify the influence of endohyphal bacteria on the abilities of fungi to colonise and alter the viability and germination of seeds. We focused on five species of neotropical pioneer trees to evaluate the effects of six fungi that were (a) naturally infected with endohyphal bacteria and (b) cured of bacteria by cultivation on antibiotic-containing media. We found that endohyphal bacteria had little influence on seed colonisation by fungi. Seeds infected by fungi with endohyphal bacteria responded similarly in terms of viability and germination to uninoculated controls. However, fungi cured of endohyphal bacteria reduced seed survival and germination in some plant species. Thus in general, endohyphal bacteria reduced negative impacts of fungi on seeds. These results lay the groundwork for future investigations to determine whether soil management to manipulate endohyphal bacterial infection of soil fungi could alter weed seedbank dynamics.

Technical Abstract: Outcomes of plant-fungus interactions can be influenced by the presence of microbes such as endohyphal bacteria, which live within fungal hyphae and can alter fungal phenotypes profoundly. Endohyphal bacteria are important symbionts of soilborne fungi that associate with plants, often providing benefits to their fungal hosts and influencing plant-fungus interactions. Seeds are the primary mode of reproduction for most plants, and their interactions with soilborne fungi are key to plant demography and community structure. As such, endohyphal bacteria affecting seed-infecting fungi may be important in plant ecology, particularly in tropical forests where fungi are the dominant source of seed mortality in the soil. Here, we conducted the first experiments to date that quantify the influence of endohyphal bacteria on the abilities of fungi to colonise and alter the viability and germination of seeds. We focused on five species of neotropical pioneer trees to evaluate the effects of six fungi that were (a) naturally infected with endohyphal bacteria and (b) cured of bacteria by cultivation on antibiotic-containing media. We found that endohyphal bacteria had little influence on seed colonisation by fungi. Seeds infected by fungi with endohyphal bacteria responded similarly in terms of viability and germination to uninoculated controls. However, fungi cured of endohyphal bacteria reduced seed survival and germination in some plant species. Thus in general, endohyphal bacteria reduced negative impacts of fungi on seeds. Context-dependent outcomes resulting from particular plant-fungus-bacterium trios suggest cryptic species interactions that can define seed fate, thus shedding light on an understudied but important component of plant demography in tropical forests.