Ciliate-generated advective seawater transport supplies chemoautotrophic ectosymbionts

Abstract

Variations of [O2] and [H2S] in seawater surrounding laboratory-reared sessile ciliates with ectosymbiotic chemoautotrophic bacteria were studied at high spatial and temporal resolutions using amperometric microsensors. We show how suspension feeding by the colonial Zoothamnium niveum and the solitary Vorticella sp. in the chemocline (O2/H2S-interface) of near-natural and artificial H2S-releasing substrates generates the physico-chemical microenvironment for the ectobiotic bacteria. Continuous recordings revealed a steep increase of [O2] and decrease of [H2S] in the proximal region of Z. niveum colonies during rapid stalk contraction. Hydrogen sulphide concentrations 2.5 mm above the substrate (upper end of the fully extended colony) increased when the contracted colony extended, followed by a decrease after the colony attained the fully upright position. Multiple contractions without complete extension successively transported sulphidic seawater upwards. The solitary Vorticella sp. maintained high ambient [O2] and low [H2S] 350 μm above the H2S-releasing membrane by generating a vertical flow field that drew seawater from above toward the ciliate. Oxygen concentration at the proximal part of Vorticella sp. did not increase during contraction, whereas during slow extension deoxygenated seawater was transported upwards and rapidly mixed with the surrounding oxygenated seawater when the ciliate started to beat its cilia. In both species rapid stalk contraction and subsequent slow extension enhanced the mixing of oxygenated and deoxygenated, H2S-containing seawater; the feeding currents (toroidal vortices) drew the surrounding seawater within reach of the zooid's external surface at high speed. It is suggested that this advective fluid transport supplies the ectobiotic bacteria with O2 and H2S simultaneously. The high fluid velocity may cause a decrease in cell boundary layer thickness, thereby enhancing rates of nutrient uptake by the ectobiotic bacteria.