What keeps us together? Maintenance and termination of the thiotrophic symbiosis between the ciliate Zoothamnium niveum and Cand. Thiobios zoothamnicoli

Evolutionary theory of cooperation defines inter-species cooperation (mutualism) as mutual beneficial association, in which benefits received from the partner exceed the costs incurred. However, empirical data are extremely scarce. They require model systems, which can be cultivated and experimentally manipulated. Among the thiototrophic (sulfur-oxidizing, chemolithoautotrophic) symbioses only two systems, the lucinid bivalves and the colonial ciliates have been successfully cultivated so far. The ciliate Zoothamnium niveum and its thiotrophic ectosymbiont Candidatus Thiobios zoothamnicoli covering the surface of the feather-like host colony is especially suited for testing what are the benefits provided by the partners and under which conditions mutualism is maintained. This symbiosis colonizes shallow-water whale falls, plant debris such as mangrove peat, degrading seagrass, or wood. It grows extremely fast and reproduces rapidly under controlled conditions in flow-through aquaria. In a set of cultures, we measured the growth of the colony and the frequency of dividing symbionts to estimate host and symbiont fitness. Cultivations with normoxic seawater (274 µmol/L O2) were performed to experimentally inhibit chemoautotrophy and thus simulated a defecting symbiont. After two days, symbiont fitness decreased significantly compared to cultures under normoxic conditions (264 µmol/L O2) supplemented with 25 µmol/L ΣH2S. After seven days, this condition led to a breakdown of the association. The aposymbiotic host survived, but suffered a significant decrease in host fitness compared to sulfide-supplemented cultures. Whether the decrease in symbiont fitness after two days and the loss of symbionts after seven days was due to host sanctions, partner fidelity feedback (a mechanism intrinsically linking the benefits of both partners), or was a consequence of the experimental setup has yet to be studied. In addition, 3 h pulse and 3 h pulse followed by 12 h and 24 h chase tissue autoradiography experiments with 14C bicarbonate under sulfide-supplemented conditions were performed. Translocation of fixed organic carbon from the symbiont to the host was evident as label over host tissue increasing over time during the chases. We conclude that at least one benefit the host received was organic carbon provided by the symbiont. Furthermore, a comparison between seven-day-old cultures under non-axenic and axenic sulfide-supplemented conditions and non-axenic, normoxic conditions showed under both suboptimal conditions (either excluding the free-living microbes for uptake or excluding chemoautotrophy) a reduction of host fitness to about half, compared to host fitness under sulfide-supplemented conditions. Thus, we conclude that host nourishment comes from translocation of organic carbon provided by the symbionts and from feeding on free-living microbes in about equal shares. These first experimental manipulations of a cultivable thiotrophic model system proved extremely useful in understanding under which conditions mutualism is maintained and terminated. In nature the habitat of the symbiosis is a transient environment. Sulfide flow is highly fluctuating and may stop after some time. Our experiments predict a loss of symbionts but survival of aposymbiotic hosts upon sulfide cessation. However, so far neither aposymbiotic hosts nor a free-living symbiont population have been found yet, but have not been searched for intensively either.

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First Name: 
Jean-Marie
Last Name: 
Volland
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00436765564148
Affiliation: 
University of Vienna - Dpt Marine Biology
First Name: 
Salvador
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Espada-Hinojosa
Affiliation: 
University of Vienna - Dpt Marine Biology
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Judith
Last Name: 
Drexel
Affiliation: 
University of Vienna - Dpt Marine Biology
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Ingrid
Last Name: 
Kolar
Affiliation: 
University of Vienna - Dpt Marine Biology
First Name: 
Christian
Last Name: 
Rinke
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University of Vienna - Dpt Marine Biology
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Monika
Last Name: 
Bright
Affiliation: 
University of Vienna - Dpt Marine Biology
Choose keywords that are most applicable to your abstract. (Three maximum.): 
Trophic relations (including symbiosis)
Abstract ID: 
CBE5-152