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Chemosynthesis is the basis for symbioses between bacteria and animals forming rich ecosystems in the dark of the deep sea. However, chemosynthesis also fuels symbioses in shallow-water sediments. One group of such coastal chemosymbionts is a diverse genus of sulfur-oxidizing gammaproteobacteria called "Candidatus Thiosymbion". The symbiotic lifestyles of ‘Ca. Thiosymbion’ differ across their three very distantly related host groups: The bacteria are ectosymbionts on stilbonematine nematodes, extracellular endosymbionts in gutless oligochaetes, and intracellular endosymbionts in Astomonema nematodes. In this study, we investigated how these three distinct lifestyles in such closely related symbionts have shaped their genomic content, with a focus on defense mechanisms, as we hypothesized these would be important for ectosymbionts, but less so for endosymbionts. We found that most endosymbionts lacked essential genes for type VI secretion systems, which are often used for interbacterial killing. Additionally, the numbers of CRISPR arrays and spacers, involved in antiviral defense, as well as biosynthetic gene clusters, which produce secondary metabolites often involved in defense, were greatly reduced in endosymbiotic ’Ca. Thiosymbion’. These findings suggest that for endosymbiotic "Ca. Thiosymbion", the protected environment inside their hosts allows the loss of defensive features, while these traits are important for maintaining an ectosymbiotic lifestyle.