Comparative genomics of Mollicutes-related endobacteria supports a late invasion into Mucoromycota fungi

Author:

Longley ReidORCID,Robinson AaronORCID,Liber Julian A.ORCID,Bryson Abigail E.,Morales Demosthenes P.ORCID,LaButti KurtORCID,Riley Robert,Mondo Stephen J.ORCID,Kuo AlanORCID,Yoshinaga Yuko,Daum ChrisORCID,Barry KerrieORCID,Grigoriev Igor V.ORCID,Desirò Alessandro,Chain Patrick S. G.ORCID,Bonito GregoryORCID

Abstract

AbstractDiverse members of early-diverging Mucoromycota, including mycorrhizal taxa and soil-associated Mortierellaceae, are known to harbor Mollicutes-related endobacteria (MRE). It has been hypothesized that MRE were acquired by a common ancestor and transmitted vertically. Alternatively, MRE endosymbionts could have invaded after the divergence of Mucoromycota lineages and subsequently spread to new hosts horizontally. To better understand the evolutionary history of MRE symbionts, we generated and analyzed four complete MRE genomes from two Mortierellaceae genera: Linnemannia (MRE-L) and Benniella (MRE-B). These genomes include the smallest known of fungal endosymbionts and showed signals of a tight relationship with hosts including a reduced functional capacity and genes transferred from fungal hosts to MRE. Phylogenetic reconstruction including nine MRE from mycorrhizal fungi revealed that MRE-B genomes are more closely related to MRE from Glomeromycotina than MRE-L from the same host family. We posit that reductions in genome size, GC content, pseudogene content, and repeat content in MRE-L may reflect a longer-term relationship with their fungal hosts. These data indicate Linnemannia and Benniella MRE were likely acquired independently after their fungal hosts diverged from a common ancestor. This work expands upon foundational knowledge on minimal genomes and provides insights into the evolution of bacterial endosymbionts.

Funder

U.S. Department of Energy

National Science Foundation

United States Department of Agriculture | National Institute of Food and Agriculture

This work was performed, in part, at the Center for Integrated Nanotechnologies, an Office of Science User Facility operated for the U.S. Department of Energy (DOE) Office of Science.

Publisher

Springer Science and Business Media LLC

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology,Medicine (miscellaneous)

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