A Review of Protist Grazing Below the Photic Zone Emphasizing Studies of Oxygen-Depleted Water Columns and Recent Applications of In situ Approaches

Abstract

Little is still known of the impacts of protist grazing on bacterioplankton communities in the dark ocean. Furthermore, the accuracy of assessments of in situ microbial activities, including protist grazing, can be affected by sampling artifacts introduced during sample retrieval and downstream manipulations. Potential artifacts may be increased when working with deep-sea samples or samples from chemically unique water columns such as oxygen minimum zones (OMZs). OMZs are oxygen-depleted regions in the ocean, where oxygen concentrations can drop to <20 µM. These regions are typically located near eastern boundary upwelling systems and currently occur in waters occupying below about 8% of total ocean surface area, representing ∼1% of the ocean's volume. OMZs have a profound impact not only on the distribution of marine Metazoa, but also on the composition and activities of microbial communities at the base of marine food webs. Here we present an overview of current knowledge of protist phagotrophy below the photic zone, emphasizing studies of oxygen-depleted waters and presenting results of the first attempt to implement new technology for conducting these incubation studies completely in situ (the Microbial Sampling-Submersible Incubation Device, MS-SID). We performed 24-h incubation experiments in the Eastern Tropical South Pacific (ETSP) OMZ. This preliminary study shows that up to 28% of bacterial biomass may be consumed by protists in waters where oxygen concentrations were down to ∼4.8 µM and up to 13% at a station with nitrite accumulation where oxygen concentrations were undetectable. Results also show that shipboard measurements of grazing rates were lower than rates measured from the same water using the MS-SID, suggesting that in situ experiments help to minimize artifacts that may be introduced when conducting incubation studies using waters collected from below the photic zone, particularly from oxygen-depleted regions of the water column.

Protistan grazing impacts microbial communities and carbon cycling at deep-sea hydrothermal vents

“…Commensurate with typical declining concentrations of prokaryotes with ocean depth, deep-sea grazing rates in this study were lower relative to those measured in seawater from euphotic regions (10,25). However, when the microbial community biomass is taken into .…”

“…Free-living heterotrophic protists may adapt to low prey encounter rates, due to decreased microbial biomass in the deep sea, by associating with sinking particles or localized habitats with more abundant prey (6, 23). Transition zones such as redoxclines are also sites of comparatively higher grazing pressure since they host a more diverse and abundant prokaryotic community due to the presence of diverse sources of carbon and energy (8, 10, 24). In one of the only other studies to quantify deep-sea predation pressure, protistan grazing within a deep-sea halocline (3500 m; above the hypersaline Urania Basin in the Eastern Mediterranean Sea) was calculated to be over 13,500 cells ml -1 hour -1 , in contrast to 10-390 cells ml -1 hour -1 in the water column outside the influence of the halocline (100-3000 m; 9).…”

“…Assessments of grazing in the mesopelagic and dark ocean have found that rates of consumption decrease with depth and correspond to bacterial abundance (7, 8). Therefore, at sites of increased biological activity and microbial biomass, such as areas of redox stratification, protistan grazing is higher relative to the rest of the water column (9, 10). Comparable data have been lacking from deep-sea hydrothermal vents, where the relatively high microbial biomass and rates of primary productivity suggest protistan grazing should be a significant source of microbial mortality and carbon transfer.…”

Microzooplankton Communities in a Changing Ocean: A Risk Assessment

“…Although limited literature exists regarding the effects of climate-driven deoxygenation on microzooplankton, some observational and experimental data may help to anticipate its effects. The study of OMZs in the dark ocean has revealed high abundances of ciliates [189], and even under these seemingly hostile conditions, these organisms can attain a high degree of bacterivory [190]. However, similar to pH, the response of microzooplankton to oxygen concentration is species-specific, denoting the existence of diverse specialized oxygen niches among com-munities [109,191,192].…”

Seafloor incubation experiment with deep-sea hydrothermal vent fluid reveals effect of pressure and lag time on autotrophic microbial communities

“…This avoids biases related to sample collection lag and depressurization, although other experimental artifacts, such as bottle effects still remain (reviewed in McQuillan and Robidart 2017, Ottesen 2016). This includes the automated micro-laboratory designed to allow one to conduct multiple (in-series) tracer incubation studies during cabled or free-drifting deployments (Lippsett 2014, Taylor et al 1993, Taylor et al 1983, Taylor and Doherty 1990), as well as a modification of the instrument termed the Microbial Sampler-Submersible Incubation Device (MS-SID), allowing for in situ grazing incubation experiments together with in situ microbial sampling and preservation (Pachiadaki et al 2016; Edgcomb et al 2016; Medina et al 2017). Another instrument is the Environmental Sample Processor (ESP) unit which includes a molecular component that carries out sample homogenization and subsequent detection of particular microbial groups using quantitative PCR, sandwich hybridization, or competitive ELISA (Scholin 2018).…”