Mitochondria and Wolbachia titers are positively correlated during maternal transmission

Abstract

Mothers provide their offspring with symbionts. Maternally transmitted, intracellular symbionts must disperse from mother to offspring with other cytoplasmic elements, like mitochondria. Here, we investigated how the intracellular symbiont Wolbachia interacts with mitochondria during maternal transmission. Mitochondria and Wolbachia may interact antagonistically and compete as each population tries to ensure its own evolutionary success. Alternatively, mitochondria and Wolbachia may cooperate as both benefit from ensuring the fitness of the mother. We characterized the relationship between mitochondria and Wolbachia titers in ovaries of Drosophila melanogaster. We found that mitochondria and Wolbachia titers are positively correlated in common laboratory genotypes of D. melanogaster. We attempted to perturb this covariation through the introduction of Wolbachia variants that colonize at different titers. We also attempted to perturb the covariation through manipulating the female reproductive tract to disrupt maternal transmission. Finally, we also attempted to disrupt the covariation by knocking down gene expression for two loci involved in mitochondrial metabolism: NADH dehydrogenase and a mitochondrial transporter. Overall, we find that mitochondria and Wolbachia titers are commonly positively correlated, but this positive covariation is disrupted at high titers of Wolbachia. Our results suggest that mitochondria and Wolbachia have likely evolved mechanisms to stably coexist, but the competitive dynamics change at high Wolbachia titers. We provide future directions to better understand how their interaction influences the maintenance of the symbiosis.

Wolbachia and Sirtuin-4 interaction is associated with alterations in host glucose metabolism and bacterial titer

“…A recent study demonstrated a positive correlation between Wolbachia and mitochondrial titers in the ovarian tissue of distinct Drosophila and Wolbachia genotypes, with uninfected individuals displaying similar mitochondrial titers as infected flies [ 82 ]. Additionally, Wolbachia titers were unaffected by a decrease in mitochondrial titer, as evidenced by knockdown of mitochondrial genes.…”

“…Further work exploring the impact of manipulating distinct mitochondrial genes on Wolbachia density, in the context of sirt-4 would be of great importance, given the existence of multiple factors affecting mitochondrial energetics in the host [ 83 ]. For instance, the work of Henry [ 82 ] differs from a previous study in which knockdown of the mitochondrial gene NADH dehydrogenase, an enzyme responsible for the conversion of NADH to its oxidized form NAD + (a key substrate in which sirtuin activity relies on), led to a significant reduction in Wolbachia load [ 84 ].…”

Recently introducedWolbachiareduces bacterial species richness and reshapes bacterial community structure inNilaparvata lugens

“…11,41,42 The evolutionary wileyonlinelibrary.com/journal/ps trajectory of Wolbachia with the host may be obligate symbiosis and it may become an organelle, such as mitochondria. 43 Moreover, Wolbachia reduces species richness but not the evenness of other bacteria, indicating that Wolbachia affects the absolute abundance of other bacteria but not bacterial variation. We speculate that the impact of the recently introduced wStri on bacterial diversity will gradually decrease over future long-term coevolution.…”

“…However, in most species, the hosts have only decreased fitness after introducing or removing facultative endosymbionts 11,41,42 . The evolutionary trajectory of Wolbachia with the host may be obligate symbiosis and it may become an organelle, such as mitochondria 43 . Moreover, Wolbachia reduces species richness but not the evenness of other bacteria, indicating that Wolbachia affects the absolute abundance of other bacteria but not bacterial variation.…”

Chorthippus parallelus and Wolbachia: Overlapping Orthopteroid and Bacterial Hybrid Zones

“…Since Wolbachia is a strictly cytoplasmic element, it has to establish a sophisticated dialogue not only with the organelles, but also with the nucleus, and even with other infectious organisms, such as the WO phage (LePage et al, 2017). This leads to frequently complex relations with the mitochondria, for example, which may sweep to cytonuclear incompatibilities (Henry and Newton, 2018). The reproductive barriers induced by this bacterium have led it to be considered a speciation agent under some circumstances (Bordenstein et al, 2001; Brucker and Bordenstein, 2012).…”