Many inherited bacteria can be found outside of cells in a hostile immune environment

The conjecture that intracellular lifestyle reduces the interaction with host innate immunity seems broadly fair. However, does this mean that inherited symbionts simply do not interact with the immune system? It is, in fact, commonly observed that many symbionts have both intra- and extracellular phases (Moran et al., 2005b), in some cases moving outside of cells during certain life-history phases. Other microbes that are maternally inherited symbionts, such as Arsenophonus, have an extracellular location (Huger et al., 1985).

Movement of intracellular symbionts into the haemolymph during certain host life-history stages is observed commonly. Primary symbionts move from the bacteriome during various phases of the host life history. For instance, SZPE, a gamma pro-teobacterium and the required symbiont of weevils, is extensively found free in the haemocoel during nymphal maturation, alongside expression of inv/ spa genes associated with entry into cells (Dale et al., 2002). In lice, Riesia bacteria usually found intracellularly within bacteriomes are observed to undergo two extracellular migrations during their host's life history (Perotti et al., 2007). Reproductive parasites such as Wolbachia can be observed on the exterior of ovarioles, migrating into forming oocytes through the germ-line stem cells following microinjection (Frydman et al., 2006), and the male-killing Flavobacteria in ladybirds can be observed adjacent to the sheath surrounding the host ovary (Hurst et al., 1999).

Other bacteria live both inside and outside cells. A dark field micrograph of Drosophila haemolymph can reveal thousands of Spiroplasma poulsonii free in the haemolymph. While spiroplasmas can be found in cells (notably, in the embryo), the haemolymph is likely the usual habitat for spiroplasmas outside the S. ixodetis clade. Secondary symbionts like S. symbiotica and H. defensa are found in the cells surrounding the bacteriome, but are also found widely in other host tissues, and are found free in the haemolymph (Moran et al, 2005b). Indeed, this location may be a requirement for them to display their antiparasite defence capability. Sodalis is also found in diverse tissues, including the haemo-lymph, and has both extracellular and intracellular phases (Cheng and Aksoy, 1999).

Finally, some inherited bacteria are primarily extracellular. Arsenophonus nasoniae, which is largely transovarially transmitted, invades its host by its mouth each generation, enters through the gut wall, and then is transmitted again at oviposition alongside the egg (although not in it). It can be transmitted horizontally on superparasitism of a host fly pupa by more than one wasp individual (Skinner, 1985), and this represents an intermediate between infectious transmission and vertically transmitted symbiosis. This transmission process is also mirrored in some Wolbachia strains, which can cross between host individuals following co-infection of a host by two parasitoid individuals.

These observations indicate that many symbionts are found outside cells at some point in their life history, and that this will lead to them being exposed to interaction with the host immune system. For parasites, avoidance of immune system activity must be a property of the bacterium. For beneficial symbionts, which the host has an interest in maintaining, it may be a property of the bacterium, the host, or both.

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