Associated bacterial communities, confrontation studies, and comparative genomics reveal important interactions between Morchella with Pseudomonas spp

Guillaume Cailleau; Buck T Hanson; Melissa Cravero; Sami Zhioua; Patrick Hilpish; Celia Ruiz; Aaron J Robinson; Julia M Kelliher; Demosthenes Morales; La Verne Gallegos-Graves; Gregory Bonito; Patrick S G Chain; Saskia Bindschedler; Pilar Junier

doi:10.3389/ffunb.2023.1285531

Associated bacterial communities, confrontation studies, and comparative genomics reveal important interactions between Morchella with Pseudomonas spp

Front Fungal Biol. 2023 Dec 13:4:1285531. doi: 10.3389/ffunb.2023.1285531. eCollection 2023.

Affiliations

¹ Laboratory of Microbiology, University of Neuchâtel, Neuchâtel, Switzerland.
² Bioscience Division, Los Alamos National Laboratory, Los Alamos, NM, United States.
³ Center for Integrated Nanotechnologies, Los Alamos National Laboratory, Los Alamos, NM, United States.
⁴ Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI, United States.

Abstract

Members of the fungal genus Morchella are widely known for their important ecological roles and significant economic value. In this study, we used amplicon and genome sequencing to characterize bacterial communities associated with sexual fruiting bodies from wild specimens, as well as vegetative mycelium and sclerotia obtained from Morchella isolates grown in vitro. These investigations included diverse representatives from both Elata and Esculenta Morchella clades. Unique bacterial community compositions were observed across the various structures examined, both within and across individual Morchella isolates or specimens. However, specific bacterial taxa were frequently detected in association with certain structures, providing support for an associated core bacterial community. Bacteria from the genus Pseudomonas and Ralstonia constituted the core bacterial associates of Morchella mycelia and sclerotia, while other genera (e.g., Pedobacter spp., Deviosa spp., and Bradyrhizobium spp.) constituted the core bacterial community of fruiting bodies. Furthermore, the importance of Pseudomonas as a key member of the bacteriome was supported by the isolation of several Pseudomonas strains from mycelia during in vitro cultivation. Four of the six mycelial-derived Pseudomonas isolates shared 16S rDNA sequence identity with amplicon sequences recovered directly from the examined fungal structures. Distinct interaction phenotypes (antagonistic or neutral) were observed in confrontation assays between these bacteria and various Morchella isolates. Genome sequences obtained from these Pseudomonas isolates revealed intriguing differences in gene content and annotated functions, specifically with respect to toxin-antitoxin systems, cell adhesion, chitinases, and insecticidal toxins. These genetic differences correlated with the interaction phenotypes. This study provides evidence that Pseudomonas spp. are frequently associated with Morchella and these associations may greatly impact fungal physiology.

Keywords: bacteriome; fruiting body; morel; mycelium; sclerotia.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was performed under the mandate “Analysis of the invasive potential of Morels” contract number 00.5005.PZ/3A7FD7C3E with the Federal Office for the Environment from Switzerland. Additional support was provided by a Science Focus Area Grant from the U.S. Department of Energy (DOE), Biological and Environmental Research (BER), Biological System Science Division (BSSD) under grant number LANLF59T. GB also acknowledges US National Science Foundation grant DEB-1946445.