Host-symbiont stress response to lack-of-sulfide in the giant ciliate mutualism

Abstract

The mutualism between the thioautotrophic bacterial ectosymbiont Candidatus Thiobius zoothamnicola and the giant ciliate Zoothamnium niveum thrives in a variety of shallow-water marine environments with highly fluctuating sulfide emissions. To persist over time, both partners must reproduce and ensure the transmission of symbionts before the sulfide stops, which enables carbon fixation of the symbiont and nourishment of the host. We experimentally investigated the response of this mutualism to depletion of sulfide. We found that colonies released some initially present but also newly produced macrozooids until death, but in fewer numbers than when exposed to sulfide. The symbionts on the colonies proliferated less without sulfide, and became larger and more rod-shaped than symbionts from freshly collected colonies that were exposed to sulfide and oxygen. The symbiotic monolayer was severely disturbed by growth of other microbes and loss of symbionts. We conclude that the response of both partners to the termination of sulfide emission was remarkably quick. The development and the release of swarmers continued until host died and thus this behavior contributed to the continuation of the association.

Zoothamnium mariella sp. nov., a marine, colonial ciliate with an atypcial growth pattern, and its ectosymbiont Candidatus Fusimicrobium zoothamnicola gen. nov., sp. nov.

“…Thiobius zoothamnicola, only thrives on substrates composed of or located near decaying organic matter [ 21 – 23 , 31 , 90 – 92 ]. Z. niveum ’s ectosymbiont depends on sulfide, released during degradation of organic matter [ 73 ], as an electron donor as well as oxygen as electron acceptor [ 23 , 24 ] to energize inorganic carbon fixation [ 25 ]. Additionally, Z. niveum and its ectosymbiont have so far been detected in temperate waters only during summer [ 23 – 25 , 92 ], as the availability of sulfide in the ocean is strongly temperature dependent [ 93 , 94 ] In the tropics and subtropics, the symbiosis can be found throughout the year [ 22 , 31 , 77 , 90 , 91 ].…”

“…Within the main classes of ciliates, symbionts may colonize not only the inside of host cells, but also the host surface as ectosymbionts [10]. A well-studied ectosymbiosis is that between the peritrichous ciliate Zoothamnium niveum and its thiotrophic ectosymbiont Candidatus Thiobius zoothamnicola [21][22][23][24][25][26][27][28][29][30][31]. This bacterial symbiont oxidizes sulfide [23,24] to generate energy for inorganic carbon fixation and subsequently transfer organic carbon to its ciliate host [25].…”

“…A well-studied ectosymbiosis is that between the peritrichous ciliate Zoothamnium niveum and its thiotrophic ectosymbiont Candidatus Thiobius zoothamnicola [21][22][23][24][25][26][27][28][29][30][31]. This bacterial symbiont oxidizes sulfide [23,24] to generate energy for inorganic carbon fixation and subsequently transfer organic carbon to its ciliate host [25]. Besides Z. niveum, only few other Zoothamnium species are known to be colonized by ectosymbiotic bacteria [32][33][34][35][36][37][38][39][40].…”

Cellular interactions and evolutionary origins of endosymbiotic relationships with ciliates

“…Additionally, sessile ciliates like Zoothamnium niveum inhabit sulfur-rich environments with thiotrophic ectosymbionts “ Candidatus Thiobios zoothamnicoli” ( Fig. 4D ) [ 42 , 195 , 196 ]. These symbionts fix carbon and transfer it to the host cell under oxic and sulfidic conditions, but decline in the absence of sulfide, leading to limited host growth and lifespan [ 197 ].…”