The role of dissolved infochemicals in mediating predator-prey interactions in the heterotrophic dinoflagellate Oxyrrhis marina

Breckels, Mark N.; Roberts, Edward; Archer, Stephen D.; Malin, Gill; Steinke, Michael

doi:10.1093/plankt/fbq114

Cited by 36 publications

(46 citation statements)

References 70 publications

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“…Investigations of protozoan feeding in planktonic con- texts have shown that selective feeding is influenced by a complex range of factors, including prey cell size (16,50), motility (38), cell surface properties (41), and biochemical composition (57). Additionally, dissolved chemical cues are of recognized importance in planktonic protist feeding interactions (9,56). The two bacteria included in this study are Gram-negative rods with similar cell dimensions (approximately 1.5 m long and 0.5 to 1.0 m in diameter; 70) and were embedded in biofilms, making it unlikely that either prey dimensions or motility was important in this case.…”

Section: Discussionmentioning

confidence: 99%

Preferential Feeding by the Ciliates Chilodonella and Tetrahymena spp. and Effects of These Protozoa on Bacterial Biofilm Structure and Composition

Dopheide

Lear

Stott

et al. 2011

Appl Environ Microbiol

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Protozoa are important components of microbial food webs, but protozoan feeding preferences and their effects in the context of bacterial biofilms are not well understood. The feeding interactions of two contrasting ciliates, the free-swimming filter feeder Tetrahymena sp. and the surface-associated predator Chilodonella sp., were investigated using biofilm-forming bacteria genetically modified to express fluorescent proteins. According to microscopy, both ciliates readily consumed cells from both Pseudomonas costantinii and Serratia plymuthica biofilms. When offered a choice between spatially separated biofilms, each ciliate showed a preference for P. costantinii biofilms. Experiments with bacterial cell extracts indicated that both ciliates used dissolved chemical cues to locate biofilms. Chilodonella sp. evidently used bacterial chemical cues as a basis for preferential feeding decisions, but it was unclear whether Tetrahymena sp. did also. Confocal microscopy of live biofilms revealed that Tetrahymena sp. had a major impact on biofilm morphology, forming holes and channels throughout S. plymuthica biofilms and reducing P. costantinii biofilms to isolated, grazing-resistant microcolonies. Grazing by Chilodonella sp. resulted in the development of less-defined trails through S. plymuthica biofilms and caused P. costantinii biofilms to become homogeneous scatterings of cells. It was not clear whether the observed feeding preferences for spatially separated P. costantinii biofilms over S. plymuthica biofilms resulted in selective targeting of P. costantinii cells in mixed biofilms. Grazing of mixed biofilms resulted in the depletion of both types of bacteria, with Tetrahymena sp. having a larger impact than Chilodonella sp., and effects similar to those seen in grazed single-species biofilms.

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Section: Discussionmentioning

confidence: 99%

Preferential Feeding by the Ciliates Chilodonella and Tetrahymena spp. and Effects of These Protozoa on Bacterial Biofilm Structure and Composition

Dopheide

Lear

Stott

et al. 2011

Appl Environ Microbiol

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“…In this study, the predators were the dinoflagellate Oxyrrhis marina , a very small animal, about 40 μm long and 15 μm wide (Breckels et al . ; Roberts et al . ), and its prey were the even smaller algae Rhodomonas sp, which are roughly spherical in shape with a diameter of about 8 μm.…”

Section: Testing the Lévy Hypothesismentioning

confidence: 99%

“…Assuming a chemical ‘phycosphere’ surrounding each Rhodomonas cell equal in width to up to four times its radius, enabling detection by an Oxyrrhis when its path intersects this phycospehere (Breckels et al . ), the effective radius of detection for Oxyrrhis searching for Rhodomonas would be at most about 27·5 μm (i.e. half Oxyrrhis width plus five times Rhodomonas radius).…”

Section: Testing the Lévy Hypothesismentioning

confidence: 99%

Understanding movements of organisms: it's time to abandon the Lévy foraging hypothesis

2014

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Summary1. Interest in Levy walks within the context of movement of organisms has recently soared, with some now referring to this approach as the Levy walk/flight paradigm. The principal assumptions, taken from the world of physics, have been that organisms searching for food or some other resource adopt random walks, whereby the direction of each successive step in the walk is chosen at random from the complete circle and the length of each step, unless terminated through resource encounter, is chosen from a Levy probability distribution with a particular exponent l. The additional assumption that organisms forage optimally, such that l maximizes the rate of resource encounter, has led to the so-called Levy foraging hypothesis, with many attempts to test it. 2. However, the Levy walk model is unrealistic, especially as it omits directionality between successive steps, a typical feature of movements of individual organisms at spatial scales relevant to their movement decisions. It also results in lower foraging efficiency than other more realistic models and the evidence that organisms actually 'do the Levy walk' is weak to non-existent, despite claims to the contrary. Early optimal foraging studies of movements of organisms and a new generation of movement models avoid these problems. 3. It is therefore time to divorce the Levy walk model from optimal foraging theory, revisit some of the early optimal foraging studies of movements and pursue the new generation of movement models. However, the Levy approach may still prove useful at relatively large spatial scales, in terms of both theory and observations, especially in relation to distribution, dispersal and other population-level phenomena, and in this way biology, physics and mathematics may yet work well together.

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“…Using a lower and wider DMS concentration range (0.01–100 μM), Breckels et al . () found no significant motile chemosensory response in O. marina (CCAP 1133/5). Why heterotrophic protists, phytoplankton and bacteria are attracted to DMS is not fully understood.…”

Section: Resultsmentioning

confidence: 87%

Modelling dimethylsulfide diffusion in the algal external boundary layer: implications for mutualistic and signalling roles

Lavoie

Galí

Sévigny

et al. 2018

Environmental Microbiology

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Summary Dimethylsulfide (DMS), a dominant organic sulfur species in the surface ocean, may act as a signalling molecule and contribute to mutualistic interactions between bacteria and marine algae. These proposed functions depend on the DMS concentration in the vicinity of microorganisms. Here, we modelled the DMS enrichment at the surface of DMS‐releasing marine algal cells as a function of DMS production rate, algal cell radius and turbulence. Our results show that the DMS concentration at the surface of unstressed phytoplankton with low DMS production rates can be enriched by <1 nM, whereas for mechanically stressed algae with high activities of the enzyme DMSP‐lyase (a coccolithophore and a dinoflagellate) DMS cell surface enrichments can reach ~10 nM, and could potentially reach μM levels in large cells. These DMS enrichments are much higher than the median DMS concentration in the surface ocean (1.9 nM), and thus may attract and support the growth of bacteria living in the phycosphere. The bacteria in turn may provide photoactive iron chelators (siderophores) that enhance algal iron uptake and provide algal growth factors such as auxins and vitamins. The present study highlights new insights on the extent and impact of microscale DMS enrichments at algal surfaces, thereby contributing to our understanding of the potential chemoattractant and mutualistic roles of DMS in marine microorganisms.

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The role of dissolved infochemicals in mediating predator-prey interactions in the heterotrophic dinoflagellate Oxyrrhis marina

Cited by 36 publications

References 70 publications

Preferential Feeding by the Ciliates Chilodonella and Tetrahymena spp. and Effects of These Protozoa on Bacterial Biofilm Structure and Composition

Preferential Feeding by the Ciliates Chilodonella and Tetrahymena spp. and Effects of These Protozoa on Bacterial Biofilm Structure and Composition

Understanding movements of organisms: it's time to abandon the Lévy foraging hypothesis

Modelling dimethylsulfide diffusion in the algal external boundary layer: implications for mutualistic and signalling roles

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