Meiofauna Meets Microbes—Chemosynthetic Symbioses

Abstract

Nutritional symbioses of meiofauna with chemosynthetic bacteria occur across the globe, from deep-sea vents and seeps to shallow water sediments. The bacteria provide nutrition to their hosts, and the hosts provide both habitat and the efficient bridging of long redox gradients. In this chapter, we summarize our current understanding of these intricate symbioses, identify knowledge gaps and point out future-oriented research directions in this expanding field. The peak species diversity of meiobenthic hosts of chemosynthetic bacteria is found in shallow water sediments towards the tropics, however in only a few higher taxa, including ciliates, platyhelminths, nematodes and oligochaetes. The degree of association ranges from ectosymbioses, subcuticular endosymbioses to intracellular endosymbioses. Independent of the association type, several modes of nutritional transfer have been documented, even a transfer of nutrients via outer membrane vesicles. The mode of symbiont transmission is independent of association type or nutrient transfer. It can be strictly vertical or a mixed mode depending on the host group, but largely remains unknown. The symbiotic life style has profound influences on morphology and functions in both partners. The mouth and several other key structures related to food uptake or excretion are reduced in members of all host phyla. Several bacterial partners exhibit a strongly modified cell biology with longitudinal division as an adaptation to secure contact with the host. The host immune system, responsible for establishment and maintenance of the symbiotic association, appears highly specific and except for the oligochaetes, allows only one microbial partner across the host phyla. The receptor and effector molecules that ensure the selective presence of the “right”, and the effective defence against the “wrong”, microbes appear convergent for both nematodes and oligochaetes. In both hosts, the symbionts appear integrated into the host defence. Diverse carbon and energy sources are exploited and the ability to use small organic molecules as carbon source puts the strict autotrophy of these symbiotic consortia in question. Mixotrophy and even heterotrophy are possible, and in addition, anaplerosis seems to play an important role in inorganic carbon acquisition. Among the symbionts, the Gammaproteobacterium Ca. Thiosymbion stands out with an extremely broad physiological spectrum that includes nitrogen fixation in some hosts. This flexibility has enabled it to associate with phylogenetically unrelated host groups and adopt all possible life styles, from ectosymbiont to intracellular endosymbiont. Frontiers and challenges of future research in this field include the still unresolved taxonomic diversity of these symbioses, their puzzling evolutionary dynamics, the lack of cultivable representatives, and the unknown scale of their global influence in permeable sediments, one of the largest global habitats.