Ciliate-generated advective seawater transport supplies chemoautotrophic ectosymbionts

Vopel, Kay; Pöhn, Martina; Sorgo, Angelika; Ott, Jörg

doi:10.3354/meps210093

Cited by 17 publications

(27 citation statements)

References 19 publications

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“…Here, the upward transport of seawater is caused by the unfolding and lifting of the bunched zooids, as illustrated in Fig. 4A-2 (Vopel et al 2001). These measurements revealed that sulphidic bottom water around the proximal region of Z. niveum colonies was displaced by oxygenated seawater from above after stalk contraction.…”

Section: Discussionmentioning

confidence: 99%

“…It was argued that rapid contraction of the ciliates increased the Reynolds number and prevented O 2 -laden seawater from being dragged along, which otherwise would push the sulphidic bottom water away before contact with the bacteria. Subsequently, this model was tested by applying fast-responding amperometric O 2 and H 2 S microelectrodes to bacteria-ciliate associations reared in the laboratory on H 2 S-releasing substrates (Vopel et al 2001). These measurements indicated that it is not the bathing of the ectobiotic bacteria alternately in anoxic, H 2 S-containing and O 2 -saturated seawater, but the cilia-generated advective seawater transport that turns the zooids external surface into an attractive microhabitat for chemoautotrophic bacteria; it was suggested that, in both ciliate species, rapid stalk contraction and subsequent slow extension merely contributed to the mixing of oxygenated and deoxygenated H 2 S-containing seawater within the substrate-seawater boundary layer.…”

Section: Introductionmentioning

confidence: 99%

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Flow microenvironment of two marine peritrich ciliates with ectobiotic chemoautotrophic bacteria

Vopel¹,

Reick²,

Arlt³

et al. 2002

Aquat. Microb. Ecol.

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The flow microenvironment of 2 marine peritrich ciliates, Vorticella sp. and Zoothamnium niveum, with ectobiotic sulfur bacteria was studied with frame-by-frame analyses of video sequences and a microsensor for fluid velocity. Both species populate the chemocline above H 2 Sreleasing mangrove peat. Vorticella sp. moves the surrounding seawater up to a horizontal and vertical distance of at least 400 µm with a maximum flow velocity of 18 mm s -1 close to its peristomial edge. The feather-shaped colonies of Z. niveum generate a unidirectional flow of seawater passing the colony perpendicular to the stalk; the convex side of the feather faces upstream. The flow velocity increased exponentially towards the colony, up to 11 mm s -1 at a distance of 100 µm. Contraction of the stalk forces the zooids of Vorticella sp. and Z. niveum towards the substrate at a high velocity of 71 and 520 mm s -1 , respectively. During contraction of Vorticella sp., only little seawater is dragged along towards the surface to which the ciliates are attached whereas the contraction of Z. niveum resulted in a clear increase in the velocity of the seawater both surrounding the colony and above the substrate. Extension of the species proceeds 700 to 1000 times more slowly than contraction, and the surrounding seawater sticks to the cells and therefore is dragged along. The measurements given here support our earlier data indicating the importance of the feeding current for the bacteria-ciliate association, i.e. the cilia beat drives H 2 S-and O 2 -containing seawater toward the zooid at high velocity and thus, supports the growth of the ectobiotic sulfide-oxidizing bacteria. Rapid movement, shrinkage (Vorticella sp.) and bunching (Z. niveum) of the zooids during stalk contraction apparently cause sufficient shear stress to abrade ectobiotic bacteria that, once suspended, could enter the feeding currents.KEY WORDS: Sulfur ectosymbioses · Chemoautotrophic bacteria · Peritrich ciliates · Vorticella · Zoothamnium niveum · Flow velocity Resale or republication not permitted without written consent of the publisher

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Flow microenvironment of two marine peritrich ciliates with ectobiotic chemoautotrophic bacteria

Vopel¹,

Reick²,

Arlt³

et al. 2002

Aquat. Microb. Ecol.

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“…According to observations on the vertical distribution of Caribbean Stilbonematinae (Laxus oneistus; Ott et al 1995) in laboratory experiments, these nematodes expose their symbionts alternately to reducing or oxidizing conditions by migrations through the chemocline in both directions (Ott et al 1991). Another strategy for providing sulfide oxidizing ectosymbionts with suitable environmental conditions has been suggested by Ott et al (1998) and modified by Vopel et al (2001) for a sedentary, feather-shaped, colonial peritrich ciliate that expands into oxygenated water and contracts into sulfidic water close to the substrate. The substrate is mangrove peat above which steep redox variations are present in the mm-range.…”

Section: Ecologymentioning

confidence: 99%

Leptonemella species (Desmodoridae, Stilbonematinae), benthic marine nematodes with ectosymbiotic bacteria, from littoral sand of the North Sea island of Sylt: taxonomy and ecological aspects

Riemann

Thiermann

Bock

2003

Helgoland Marine Research

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Leptonemella species represent a dominant element of the nematode fauna in sulfidic, deep sediment layers on the sandy shore of Sylt. Based on collections sampled here in 1991-1999, a taxonomic treatise is presented on the three co-existing species, Leptonemella aphanothecae Gerlach, 1950, the closely related L. vicina sp. nov., and L. gorgo Gerlach, 1950. The high incidence of pseudohermaphrodites in the material, mostly functional females with a male copulatory apparatus, is remarkable. The highest population densities of Leptonemella spp. (up to 73 individuals/10 ml sand) were found near polychaete burrows. Because of the great spatial and temporal variations in the oxygen/sulfide regime of these microhabitats, and because of the strong adhesive capabilities of Leptonemella spp., which can anchor themselves firmly to sand grains using caudal glands, we propose that a hemisessile life strategy is employed by these nematodes to fulfill the metabolic needs of their sulfide-oxidizing ectosymbionts.

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“…Ott et al (1998) proposed that Z. niveum supplies the bacterial symbionts with sulWde through periodic contraction into the anoxic and sulWdic diVusive boundary layer (DBL). Studies of the physical and chemical microenvironment around the colonies (Vopel et al 2001(Vopel et al , 2002(Vopel et al , 2005 could not conWrm this mechanism, but suggested that the feeding currents intercept sulWde and brings it to the symbiotic bacteria.…”

Section: Introductionmentioning

confidence: 99%

“…A trophic character of the symbiosis is suggested from observation of bacteria morphotypes in the food vacuoles (Bauer-Nebelsick et al 1996b), and by poor growth of the ciliates without ectosymbionts (Ott et al 1998;Vopel et al 2001). Ott et al (1998) proposed that Z. niveum supplies the bacterial symbionts with sulWde through periodic contraction into the anoxic and sulWdic diVusive boundary layer (DBL).…”

Section: Introductionmentioning

confidence: 99%

Sulfide assimilation by ectosymbionts of the sessile ciliate, Zoothamnium niveum

et al. 2009

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We investigated the constraints on sulWde uptake by bacterial ectosymbionts on the marine peritrich ciliate Zoothamnium niveum by a combination of experimental and numerical methods. Protists with symbionts were collected on large blocks of mangrove-peat. The blocks were placed in a Xow cell with Xow adjusted to in situ velocity. The water motion around the colonies was then characterized by particle tracking velocimetry. This shows that the feather-shaped colony of Z. niveum generates a unidirectional Xow of seawater through the colony with no recirculation. The source of the feeding current was the free-Xowing water although the size of the colonies suggests that they live partly submerged in the diVusive boundary layer. We showed that the Wltered volume allows Z. niveum to assimilate suYcient sulWde to sustain the symbiosis at a few micromoles per liter in ambient concentration. Numerical modeling shows that sulWde oxidizing bacteria on the surfaces of Z. niveum can sustain 100-times higher sulWde uptake than bacteria on Xat surfaces, such as microbial mats. The study demonstrates that the Wlter feeding zooids of Z. niveum are preadapted to be prime habitats for sulWde oxidizing bacteria due to Z. niveum's habitat preference and due to the feeding current. Z. niveum is capable of exploiting low concentrations of sulWde in near norm-oxic seawater. This links its otherwise dissimilar habitats and makes it functionally similar to invertebrates with thiotrophic symbionts in Wltering organs.

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Ciliate-generated advective seawater transport supplies chemoautotrophic ectosymbionts

Cited by 17 publications

References 19 publications

Flow microenvironment of two marine peritrich ciliates with ectobiotic chemoautotrophic bacteria

Flow microenvironment of two marine peritrich ciliates with ectobiotic chemoautotrophic bacteria

Leptonemella species (Desmodoridae, Stilbonematinae), benthic marine nematodes with ectosymbiotic bacteria, from littoral sand of the North Sea island of Sylt: taxonomy and ecological aspects

Sulfide assimilation by ectosymbionts of the sessile ciliate, Zoothamnium niveum

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