AUTHOR=Moore Logan D. , Ballinger Matthew J. 

TITLE=The toxins of vertically transmitted Spiroplasma

JOURNAL=Frontiers in Microbiology

VOLUME=14

YEAR=2023

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2023.1148263

DOI=10.3389/fmicb.2023.1148263

ISSN=1664-302X

ABSTRACT=<p>Vertically transmitted (VT) microbial symbionts play a vital role in the evolution of their insect hosts. A longstanding question in symbiont research is what genes help promote long-term stability of vertically transmitted lifestyles. Symbiont success in insect hosts is due in part to expression of beneficial or manipulative phenotypes that favor symbiont persistence in host populations. In <italic>Spiroplasma</italic>, these phenotypes have been linked to toxin and virulence domains among a few related strains. However, these domains also appear frequently in phylogenetically distant <italic>Spiroplasma,</italic> and little is known about their distribution across the <italic>Spiroplasma</italic> genus. In this study, we present the complete genome sequence of the <italic>Spiroplasma</italic> symbiont of <italic>Drosophila atripex</italic>, a non-manipulating member of the Ixodetis clade of <italic>Spiroplasma</italic>, for which genomic data are still limited. We perform a genus-wide comparative analysis of toxin domains implicated in defensive and reproductive phenotypes. From 12 VT and 31 non-VT <italic>Spiroplasma</italic> genomes, ribosome-inactivating proteins (RIPs), OTU-like cysteine proteases (OTUs), ankyrins, and ETX/MTX2 domains show high propensity for VT <italic>Spiroplasma</italic> compared to non-VT <italic>Spiroplasma</italic>. Specifically, OTU and ankyrin domains can be found only in VT-<italic>Spiroplasma</italic>, and RIP domains are found in all VT <italic>Spiroplasma</italic> and three non-VT <italic>Spiroplasma</italic>. These domains are frequently associated with <italic>Spiroplasma</italic> plasmids, suggesting a possible mechanism for dispersal and maintenance among heritable strains. Searching insect genome assemblies available on public databases uncovered uncharacterized <italic>Spiroplasma</italic> genomes from which we identified several <italic>spaid</italic>-like genes encoding RIP, OTU, and ankyrin domains, suggesting functional interactions among those domain types. Our results suggest a conserved core of symbiont domains play an important role in the evolution and persistence of VT <italic>Spiroplasma</italic> in insects.</p>