A symbiont's guide to the germline

Abstract

Microbial symbioses exhibit astounding adaptations, yet all symbionts face the problem of how to reliably associate with host offspring every generation. A common strategy is vertical transmission, in which symbionts are directly transmitted from the female to her offspring. The diversity of symbionts and vertical transmission mechanisms is as expansive as the diversity of eukaryotic host taxa that house them. However, there are several common themes among these mechanisms based on the degree to which symbionts associate with the host germline during transmission. In this review, we detail three distinct vertical transmission strategies, starting with associations that are transmitted from host somatic cells to offspring somatic cells, either due to lacking a germline or avoiding it. A second strategy involves somatically-localized symbionts that migrate into the germline during host development. The third strategy we discuss is one in which the symbiont maintains continuous association with the germline throughout development. Unexpectedly, the vast majority of documented vertically inherited symbionts rely on the second strategy: soma-to-germline migration. Given that not all eukaryotes contain a sequestered germline and instead produce offspring from somatic stem cell lineages, this soma-to-germline migration is discussed in the context of multicellular evolution. Lastly, as recent genomics data have revealed an abundance of horizontal gene transfer events from symbiotic and non-symbiotic bacteria to host genomes, we discuss their impact on eukaryotic host evolution.

One fly–one genome: chromosome-scale genome assembly of a single outbred Drosophila melanogaster

“…Despite the differences in read-depths relative to the nuclear genome, our assembly includes nearly full coverage of the Wolbachia genome with few apparent misassemblies (Figure 3 and Supplementary Figure S2 ). Wolbachia in particular ( 33 ), and endosymbionts more generally ( 34 ), are frequently present in host somatic tissues, likely explaining the similar abundances of Wolbachia -derived reads across sequencing libraries prepared from different parts of the fly. This suggests that in addition to nearly complete nuclear genomes, our assembly method might also be a powerful tool for investigating individual's endosymbiont communities – a fundamental consideration in arthropod biology ( 35 ).…”

Tissue Tropisms and Transstadial Transmission of a Rickettsia Endosymbiont in the Highland Midge, Culicoides impunctatus (Diptera: Ceratopogonidae)

“…The transmission routes of Rickettsia endosymbionts in biting midges are underexplored but can be informed by symbiont tissue localization. Although the maternal transmission of obligate symbionts is generally dependent on specialized cells (bacteriocytes), facultative (secondary) symbionts utilize various means to target the germ line ( 25 ). These can come in the form of cooption of yolk granules to gain entry into egg chambers via endocytosis (e.g., Spiroplasma in Drosophila melanogaster ) ( 39 ), or through the continuous association with the germ line during morphogenesis (e.g., Wolbachia in Drosophila spp.)…”

“…However, the route of migration to egg chambers by the symbiont is not clear and the tropisms to other tissues remain unexplored. Vertical transmission of nonobligate symbionts is achieved through diverse modes of germ line targeting ( 25 ). With certain Wolbachia strains of Drosophila spp., the symbiont localizes in the germ line stem cell niche continuously throughout development ( 26 – 28 ).…”

Trends in symbiont-induced host cellular differentiation

“…Often present in host germline stem cells (Russell et al 2019), Wolbachia has been shown to be capable of rescuing or maintaining this cell lineage in different host taxa. In D. melanogaster, the wMel strain of Wolbachia can rescue mutations in the germline stem cell maintenance genes sex lethal (sxl) (Starr and Cline 2002;Sun and Cline 2009) and bag of marbles (bam) (Flores et al 2015).…”