Being the most numerous, diverse and ubiquitous group of animals, the arthropods have established a wide array of interactions with bacteria. Despite their considerable potential in agriculture, health-care and pest control, exploration of these associations is limited to a few well studied associations (Bourtzis & Miller 2003), while comprehensive understanding of interactions between bacteria and arthropods generally remain underexplored, due to lack of appropriate model organisms. Our work in recent years has been therefore focused on bacterial associations in terrestrial isopod crustaceans (Fig. 1), a diverse and ubiquitous group of arthropods, with considerable ecological role, well-known biology and undemanding maintenance under laboratory conditions.

In order to expand our knowledge on isopod-bacteria associations we used a wide array of microscopic approaches on crustacean tissues including FE-SEM, TEM and fluorescence microscopy with structured illumination in combination with histochemistry, fluorescent ‘in situ’ hybridization and EDXS analytical techniques.

Beside diverse transitional bacterial microbiota inhabiting the gut, our observations revealed three groups of bacteria exhibiting specific adaptations to the isopod host as their environment. The first are filamentous gut bacteria, belonging to a novel and distant phylogenetic lineage named ‘Candidatus Bacilloplasma’ (2). These commensal developed specific attachment structures, enabling their attachment to the tips of the cuticular structures covering the inner surface of the hindgut of common woodlouse, Porcellio scaber (Fig. 2). The second specific interaction comprises the intracellular pathogen Rhabdochlamydia porcellionis (Fig. 3), which represents the first description of the Chlamydiae in arthropods (3). Studies of infection in established cell culture (4) and in the digestive glands of its natural host, isopod P. scaber (5), enabled insight into chlamydial interactions with the host and mechanisms of pathogenesis of R. porcellionis, currently recognized as emerging pathogen. The third association includes bacterial community inhabiting specialized organs, known as the calcium bodies (6,7). These chevron-shaped organs in the body cavity of trichoniscid isopods serve as transitional storage of calcium during moulting of the exoskeleton and comprise a bacterial community of phosphate-accumulating bacteria arranged in densely packed layers surrounding a mineralized core (Fig. 4). Due to involvement of the polyphosphate-accumulating bacteria in phosphorous metabolism, the latter of described isopod symbioses can be, in contrast to the previous two, described as beneficial to the host and therefore mutualistic.

Our results show that terrestrial isopods can be considered important, yet overlooked evolutionary playgrounds, which enabled specific bacterial adaptations to the arthropod hosts and the development of novel bacterial lineages. By displaying the full scope of bacterial symbiosis ranging from pathogens, over commensals to mutualists, the terrestrial isopods have considerable potential as model organisms for much needed studies on host-symbiont interactions.

References:

(1) Bourtzis K., Miller T.A. (2003): Insect symbiosis. CRC Press, 347 pp.

(2) Kostanjšek R. Štrus, J., Avguštin G. (2007). Appl. Environ. Microbiol. 73(17): 5566-5573.

(3) Kostanjšek R., Štrus J., Drobne D., Avguštin G. (2004).  Int J Syst Evol Microbiol, 54: 543-549.

(4) Sixt B.S., Kostanjšek R., Mustedanagic A., Toenshoff E.R., Horn M. (2013). Environ. Microbiol. 15(1): 2980-2993.

 (5) Kostanjšek R., Pirc Marolt T. (2015). J Invertbr. Pathol. 125: 56-67.

(6) Vittori M., Kostanjšek R., Žnidaršič N., Žagar K., Čeh M., Štrus J. (2012). J. Struct. Biol 180(1): 216-225.

(7) Vittori M., Rozman A., Gradodolnik J., Novak U., Štrus J. (2013). PloS one 8(3) 1-14, e58968.

Figures:

Fig. 1. Schematic drawing of a terrestrial isopod showing the positions of the described symbioses (DG - digestive glands, HG - hindgut, CB - calcium bodies, scale bar - 5 mm)

Bacilloplasma attached to the tip of the cuticular spine in the isopod hindgut (scale bar - 1 µm)

Diverse morphotypes of R. porcellionis in the infected digestive gland cells (scale bar 1 - µm)

Fig. 4. Lamellar structure (asterisks) of the calcium bodies comprising a dense polyphosphate- accumulating bacterial community (E - epithelium on the surface of the calcium body, scale bar - 20 µm)

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EMC Abstracts - https://emc-proceedings.com/abstract/terrestrial-isopods-as-models-for-host-symbiont-interactions/