Widespread bacterial diversity within the bacteriome of fungi

Arvin E Robinson ,Julia M Kelliher,Danaé Bregnard,Vincent Hervé,Hang N Nguyen,Demosthenes P Morales,Saskia Bindschedller,Simone Lupini,Pilar Junier,Guillaume Cailleau,Matteo Buffi,Erick S Lebrun,Luciana Jandelli Gimenes,Jamey D Young,Fabio Palmieri,Christophe Paul,Amy Zheng ,La Verne Gallegos‐Graves ,Débora F Rodrigues ,Andrea Lohberger,Karen W Davenport,Geoffrey L House,James H Werner,Aislinn Estoppey,Thomas Junier,Patrick Chain

doi:10.1038/s42003-021-02693-y

Abstract

Knowledge of associations between fungal hosts and their bacterial associates has steadily grown in recent years as the number and diversity of examinations have increased, but current knowledge is predominantly limited to a small number of fungal taxa and bacterial partners. Here, we screened for potential bacterial associates in over 700 phylogenetically diverse fungal isolates, representing 366 genera, or a tenfold increase compared with previously examined fungal genera, including isolates from several previously unexplored phyla. Both a 16 S rDNA-based exploration of fungal isolates from four distinct culture collections spanning North America, South America and Europe, and a bioinformatic screen for bacterial-specific sequences within fungal genome sequencing projects, revealed that a surprisingly diverse array of bacterial associates are frequently found in otherwise axenic fungal cultures. We demonstrate that bacterial associations with diverse fungal hosts appear to be the rule, rather than the exception, and deserve increased consideration in microbiome studies and in examinations of microbial interactions.

Highlights

Knowledge of associations between fungal hosts and their bacterial associates has steadily grown in recent years as the number and diversity of examinations have increased, but current knowledge is predominantly limited to a small number of fungal taxa and bacterial partners
Two complementary methods were used to explore the diversity of constituents of the fungal bacteriome: an amplicon community profiling survey of four independent and predominantly soilderived culture collections from three geographical origins (Europe, South America and North America), and a scan of fungal genome sequencing projects for bacterial genomic signatures
The internal transcribed spacer (ITS) rDNA region was used to characterize the diversity of 294 cultivable fungal isolates from four culture collections (Supplementary Data 1)

Summary

Introduction

Knowledge of associations between fungal hosts and their bacterial associates has steadily grown in recent years as the number and diversity of examinations have increased, but current knowledge is predominantly limited to a small number of fungal taxa and bacterial partners. Despite the growing number of examples of specific bacterial associations with isolated fungal hosts, a broader perspective of both intra and extracellular bacterial associates among the larger diversity of fungal hosts is necessary in order to understand the potential evolutionary and ecological consequences of these interkingdom interactions. To address this knowledge gap and gain a more comprehensive view of the diversity of bacterial–fungal associations, we employed two complementary approaches to identify signals of potential bacterial associates among a phylogenetically broad range of fungi. This raises a multitude of questions: how frequently do fungi serve as hosts for specialized bacteria, or as potential substrates for bacteria with broad ecological niches? To what extent are bacteria transient or more persistent in their occurrence with fungi? Considering both transient cooccurrences and more persistent associations, what are the potential roles and impacts of the bacteriome on fungi, including impacts on interactions with other microscopic (e.g. protists) or macroscopic (e.g. plants and animals) organisms?

Methods

Results

Conclusion