Abstract

ABSTRACT“Candidatus Midichloria mitochondrii” is a Gram-negative bacterium that lives in strict intracellular symbiosis with the hard tick Ixodes ricinus, forming one of the most intriguing endosymbiosis described to date. The bacterium is capable of durably colonizing the host mitochondria, a peculiar tropism that makes “Ca. Midichloria mitochondrii” a very interesting tool to study the physiology of these cellular organelles. The interaction between the symbiont and the organelle has, however, been difficult to characterize. A parallelism with the predatory bacterium Bdellovibrio bacteriovorus has been drawn, suggesting the hypothesis that “Ca. Midichloria mitochondrii” could prey on mitochondria and consume them to multiply. We studied the life cycle of the bacterium within the host oocytes using a multidisciplinary approach, including electron microscopy, molecular biology, statistics, and systems biology. Our results were not coherent with a predatory-like behavior by “Ca. Midichloria mitochondrii” leading us to propose a novel hypothesis for its life cycle. Based on our results, we here present a novel model called the “mitochondrion-to-mitochondrion hypothesis.” Under this model, the bacterium would be able to move from mitochondrion to mitochondrion, possibly within a mitochondrial network. We show that this model presents a good fit with quantitative electron microscopy data.

Highlights

  • ABSTRACT “Candidatus Midichloria mitochondrii” is a Gram-negative bacterium that lives in strict intracellular symbiosis with the hard tick Ixodes ricinus, forming one of the most intriguing endosymbiosis described to date

  • A total of 11 ticks were prepared for transmission electron microscopy (TEM), and a total of 71 oocyte sections were observed, 42 at previtellogenic (P) and 29 at late-previtellogenic (LP) development

  • All observations and counts were obtained from oocyte sections; the number of counted mitochondria and bacteria likely represent an underestimation of the real numbers per cell

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Summary

Introduction

ABSTRACT “Candidatus Midichloria mitochondrii” is a Gram-negative bacterium that lives in strict intracellular symbiosis with the hard tick Ixodes ricinus, forming one of the most intriguing endosymbiosis described to date. Mitochondria containing multiple symbionts appeared to be degraded and/or swollen, with the matrix only occupying a small portion of the entire organelle These observations led Sacchi and colleagues [9] to propose that “Ca. Midichloria mitochondrii” could have a behavior similar to that of predatory bacterium (“Bdellovibrio-like” model). In the Bdellovibrio-like model, “Ca. Midichloria mitochondrii” bacteria localized in the cytoplasm would invade noncolonized mitochondria, replicate within them, and return to the cytoplasm after mitochondrial lysis [9] This hypothesis is based on the consideration that mitochondria evolved from Gram-negative bacteria and still maintain common features with them, including a double membrane [11]

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