Diversity, specificity and phylogenetic relationships of endohyphal bacteria in fungi that inhabit tropical seeds and leaves

Authors: SHAFFER, JUSTIN - University Of Arizona; SARMIENTO, CAROLINA - Smithsonian Tropical Research; ZALAMEA, PAUL-CAMILO - Smithsonian Tropical Research; GALLERY, RACHEL - University Of Arizona; Davis, Adam; BALTRUS, DAVID - University Of Arizona; ARNOLD, E - University Of Arizona

Submitted to: Frontiers in Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/2/2016
Publication Date: 11/6/2016
Citation: Shaffer, J., Sarmiento, C., Zalamea, P., Gallery, R., Davis, A.S., Baltrus, D.A., Arnold, E.A. 2016. Diversity, specificity and phylogenetic relationships of endohyphal bacteria in fungi that inhabit tropical seeds and leaves. Frontiers in Ecology and Evolution. doi.org/10.3389/fevo.2016.00116.

Interpretive Summary: Seed-inhabiting fungi can affect soil seedbank dynamics of pioneer species, with potential implications for management of weed seedbanks. Bacteria that live inside fungi (endohyphal bacterial, EHB) can affect how fungi interact with plant leaves, but EHB have not previously been studied in seed-associated fungi. The aims of this study were to quantify EHB communities in fungi that colonize seeds of tropical pioneer trees. We found that EHB are common and diverse in seed-associated fungi, representing seven bacterial phyla. The habit of occurring in seed-associated fungi, compared to leaf-associated fungi, has not resulted in detectable differences in the evolution of EHB. Our results support the hypothesis that fungus-bacteria associations in seeds have evolved multiple times, with EHB more likely to be horizontally transmitted among fungi in the soil than vertically transmitted through maternal seed lineages. Given how widespread EHB are in seed-associated fungi, and their potential for influencing seed fate, future studies of weed seedbank dynamics should quantify the impact of EHB on weed seed survival.

Technical Abstract: Fungi that recruit to seeds in the soil can influence seed dispersal, dormancy, germination, and survival. Bacteria that inhabit fungi can alter fungal phenotypes and the outcomes of plant-fungus interactions, but their prevalence in seed-associated fungi has not been evaluated. The aims of this study were to determine the occurrence and diversity of endosymbiotic bacteria (endohyphal bacteria, EHB) in fungi that colonize seeds of pioneer trees in the soil of lowland tropical forests; to elucidate factors that structure their phylogenetic and symbiotic relationships; and to explore how different ecological modes in fungi may reflect the presence or identity of EHB. We focused on two orders of fungi that are especially common and species-rich in tropical seeds (Hypocreales and Xylariales, Ascomycota). We found that EHB are common and diverse in seed-associated fungi, representing seven bacterial phyla (including three classes of Proteobacteria). The habit of occurring in fungi associated with seeds vs. leaves has not resulted in detectable structure in the evolution of EHB. Our results are consistent with multiple origins of fungus-bacteria associations, facultative symbioses, and horizontal transmission, and argue for evaluating focal pairs to determine how particular EHB affect the establishment or maintenance of fungal lifestyles.