Phagotrophic protists are a key component of microbial communities processing leaf litter under contrasting oxic conditions

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The importance of herbivory by protists in lakes of a tropical floodplain system

Inland aquatic ecosystems play a critical role in the global carbon cycle, processing a great fraction of the organic matter coming from terrestrial ecosystems, and the microbial food web is crucial in this process. Thus, we aimed to evaluate whether the food resource of planktonic protozoa comes mainly from small primary producers or heterotrophic bacteria in tropical shallows lakes, assuming the hypothesis that, in general, picocyanobacteria would be the main food resource for protists. We also expected that the autotrophic fraction would be mainly related to protists at the surface of the environments, while the heterotrophic fraction would be more important at the lower strata of the water column. We performed size-fractionation experiments to evaluate the effects of predation of protists on heterotrophic bacteria and picocyanobacteria. We also sampled planktonic organisms at the subsurface and bottom of 20 lakes in a Neotropical floodplain. We found an herbivory preference of heterotrophic flagellates, while ciliates seem to exert a stronger impact on heterotrophic bacteria. We also found no relationship between heterotrophic bacteria and protists in the field data, whereas positive relationships between picocyanobacteria and protists were observed in environments where there was sunlight. Thus, both heterotrophic bacteria and picocyanobacteria were important components in the food webs of tropical shallow lakes. Moreover, the trophic cascade caused by zooplankton predation suggests that protists are efficient in transferring the energy from the base of microbial food webs to higher trophic levels.     

Cascading effects of larval Crucian carp introduction on phytoplankton and microbial communities in a paddy field: top-down and bottom-up controls

Effects of fish predation propagate through aquatic food webs, where the classical grazing food chain and microbial loop are interwoven by trophic interactions. The overall impact on aquatic food webs is further complicated because fish may also exert bottom-up controls through nutrient regeneration. Yet, we still have limited information about cascading effects among fish, zooplankton, phytoplankton, and microbes. In this study, we performed a mesocosm experiment to evaluate effects of fish introduction on plankton communities. Six plots were set in factorial combination with fish introduction and rice straw plowing in a paddy field, and the experiment was continued for 4 weeks. Introduction of fish significantly increased chlorophyll a concentrations in smaller size fractions (<15 μm) and abundances of filamentous bacteria (>5 μm in length) and heterotrophic nanoflagellates in 3–15 μm fraction. Microbes in 0.8–3 μm fraction showed increasing but not significant trends in response to fish introduction. These results indicate cascading effects of fish predation operating via two pathways, one through grazing food chain and the other through microbial food web. Phytoplankton community compositions shifted in similar fashion in all plots until 1 week after fish introduction, and then diverged between plots with and without fish thereafter. Bottom-up effects of fish introduction were suggested by increases of total chlorophyll a and inedible phytoplankton species in response to fish introduction. This study provides an example of how fish predation regulates biomass and structure of phytoplankton and microbial communities.     

Bacterivory and herbivory: Key roles of phagotrophic protists in pelagic food webs

Research on microbial loop organisms, heterotrophic bacteria and phagotrophic protists, has been stimulated in large measure by Pomeroy's seminal paper published in BioScience in 1974. We now know that a significant fate of bacterioplankton production is grazing by < 20-µm-sized flagellates. By selectively grazing larger, more rapidly growing and dividing cells in the bacterioplankton assemblage, bacterivores may be directly cropping bacterial production rather than simply the standing stock of bacterial cells. Protistan herbivory, however, is likely to be a more significant pathway of carbon flow in pelagic food webs than is bacterivory. Herbivores include both < 20-µm flagellates as well as > 20-µm ciliates and heterotrophic dinoflagellates in the microzooplankton. Protists can grow as fast as, or faster than their phytoplankton prey. Phototrophic cells grazed by protists range from bacterial-sized prochlorophytes to large diatom chains (which are preyed upon by extracellularly-feeding dinoflagellates). Recent estimates of microzooplankton herbivory in various parts of the sea suggest that protists routinely consume from 25 to 100% of daily phytoplankton production, even in diatom-dominated upwelling blooms. Phagotrophic protists should be viewed as a dominant biotic control of both bacteria and of phytoplankton in the sea.     

Predation on prokaryotes in the water column and its ecological implications

The oxic realms of freshwater and marine environments are zones of high prokaryotic mortality. Lysis by viruses and predation by ciliated and flagellated protists result in the consumption of microbial biomass at approximately the same rate as it is produced. Protist predation can favour or suppress particular bacterial species, and the successful microbial groups in the water column are those that survive this selective grazing pressure. In turn, aquatic bacteria have developed various antipredator strategies that range from simply 'outrunning' protists to the production of highly effective cytotoxins. This ancient predator-prey system can be regarded as an evolutionary precursor of many other interactions between prokaryotic and eukaryotic organisms.     

A size-constrained feeding-niche model distinguishes predation patterns between aquatic and terrestrial food webs

Understanding the formation of feeding links provides insights into processes underlying food webs. Generally, predators feed on prey within a certain body-size range, but a systematic quantification of such feeding niches is lacking. We developed a size-constrained feeding-niche (SCFN) model and parameterized it with information on both realized and non-realized feeding links in 72 aquatic and 65 terrestrial food webs. Our analyses revealed profound differences in feeding niches between aquatic and terrestrial predators and variation along a temperature gradient. Specifically, the predator–prey body-size ratio and the range in prey sizes increase with the size of aquatic predators, whereas they are nearly constant across gradients in terrestrial predator size. Overall, our SCFN model well reproduces the feeding relationships and predation architecture across 137 natural food webs (including 3878 species and 136,839 realized links). Our results illuminate the organisation of natural food webs and enables novel trait-based and environment-explicit modelling approaches.     

Variability in protist grazing and growth on different marine Synechococcus isolates

Grazing mortality of the marine phytoplankton Synechococcus is dominated by planktonic protists, yet rates of consumption and factors regulating grazer-Synechococcus interactions are poorly understood. One aspect of predator-prey interactions for which little is known are the mechanisms by which Synechococcus avoids or resists predation and, in turn, how this relates to the ability of Synechococcus to support growth of protist grazer populations. Grazing experiments conducted with the raptorial dinoflagellate Oxyrrhis marina and phylogenetically diverse Synechococcus isolates (strains WH8102, CC9605, CC9311, and CC9902) revealed marked differences in grazing rates-specifically that WH8102 was grazed at significantly lower rates than all other isolates. Additional experiments using the heterotrophic nanoflagellate Goniomonas pacifica and the filter-feeding tintinnid ciliate Eutintinnis sp. revealed that this pattern in grazing susceptibility among the isolates transcended feeding guilds and grazer taxon. Synechococcus cell size, elemental ratios, and motility were not able to explain differences in grazing rates, indicating that other features play a primary role in grazing resistance. Growth of heterotrophic protists was poorly coupled to prey ingestion and was influenced by the strain of Synechococcus being consumed. Although Synechococcus was generally a poor-quality food source, it tended to support higher growth and survival of G. pacifica and O. marina relative to Eutintinnis sp., indicating that suitability of Synechococcus varies among grazer taxa and may be a more suitable food source for the smaller protist grazers. This work has developed tractable model systems for further studies of grazer-Synechococcus interactions in marine microbial food webs.     

Establishment of Microbial Eukaryotic Enrichment Cultures from a Chemically Stratified Antarctic Lake and Assessment of Carbon Fixation Potential

Lake Bonney is one of numerous permanently ice-covered lakes located in the McMurdo Dry Valleys, Antarctica. The perennial ice cover maintains a chemically stratified water column and unlike other inland bodies of water, largely prevents external input of carbon and nutrients from streams. Biota are exposed to numerous environmental stresses, including year-round severe nutrient deficiency, low temperatures, extreme shade, hypersalinity, and 24-hour darkness during the winter ¹. These extreme environmental conditions limit the biota in Lake Bonney almost exclusively to microorganisms ².Single-celled microbial eukaryotes (called "protists") are important players in global biogeochemical cycling ³ and play important ecological roles in the cycling of carbon in the dry valley lakes, occupying both primary and tertiary roles in the aquatic food web. In the dry valley aquatic food web, protists that fix inorganic carbon (autotrophy) are the major producers of organic carbon for organotrophic organisms ^{4, 2}. Phagotrophic or heterotrophic protists capable of ingesting bacteria and smaller protists act as the top predators in the food web ⁵. Last, an unknown proportion of the protist population is capable of combined mixotrophic metabolism ^{6, 7}. Mixotrophy in protists involves the ability to combine photosynthetic capability with phagotrophic ingestion of prey microorganisms. This form of mixotrophy differs from mixotrophic metabolism in bacterial species, which generally involves uptake dissolved carbon molecules. There are currently very few protist isolates from permanently ice-capped polar lakes, and studies of protist diversity and ecology in this extreme environment have been limited ^{8, 4, 9, 10, 5}. A better understanding of protist metabolic versatility in the simple dry valley lake food web will aid in the development of models for the role of protists in the global carbon cycle.We employed an enrichment culture approach to isolate potentially phototrophic and mixotrophic protists from Lake Bonney. Sampling depths in the water column were chosen based on the location of primary production maxima and protist phylogenetic diversity ^{4, 11}, as well as variability in major abiotic factors affecting protist trophic modes: shallow sampling depths are limited for major nutrients, while deeper sampling depths are limited by light availability. In addition, lake water samples were supplemented with multiple types of growth media to promote the growth of a variety of phototrophic organisms.RubisCO catalyzes the rate limiting step in the Calvin Benson Bassham (CBB) cycle, the major pathway by which autotrophic organisms fix inorganic carbon and provide organic carbon for higher trophic levels in aquatic and terrestrial food webs ¹². In this study, we applied a radioisotope assay modified for filtered samples ¹³ to monitor maximum carboxylase activity as a proxy for carbon fixation potential and metabolic versatility in the Lake Bonney enrichment cultures.     

Using inhibitors to investigate the involvement of cell signaling in predation by marine phagotrophic protists

Phagotrophic protists are major consumers of microbial biomass in aquatic ecosystems. However, biochemical mechanisms underlying prey recognition and phagocytosis by protists are not well understood. We investigated the potential roles of cell signaling mechanisms in chemosensory response to prey, and in capture of prey cells, by a marine ciliate (Uronema sp.) and a heterotrophic dinoflagellate (Oxyrrhis marina). Inhibition of protein kinase signal transduction biomolecules caused a decrease in both chemosensory response and predation. Inhibition of G-protein coupled receptor signaling pathways significantly decreased chemosensory response but had no effect on prey ingestion. Inhibitor compounds did not appear to affect general cell health, but had a targeted effect. These results support the idea that cell signaling pathways known in other eukaryotic organisms are involved in feeding behavior of free-living protists.     

Fertilization alters protistan consumers and parasites in crop-associated microbiomes

Crop plants carry an enormous diversity of microbiota that provide massive benefits to hosts. Protists, as the main microbial consumers and a pivotal driver of biogeochemical cycling processes, remain largely understudied in the plant microbiome. Here, we characterized the diversity and composition of protists in sorghum leaf phyllosphere, and rhizosphere and bulk soils, collected from an 8-year field experiment with multiple fertilization regimes. Phyllosphere was an important habitat for protists, dominated by Rhizaria, Alveolata and Amoebozoa. Rhizosphere and bulk soils had a significantly higher diversity of protists than the phyllosphere, and the protistan community structure significantly differed among the three plant–soil compartments. Fertilization significantly altered specific functional groups of protistan consumers and parasites. Variation partitioning models revealed that soil properties, bacteria and fungi predicted a significant proportion of the variation in the protistan communities. Changes in protists may in turn significantly alter the compositions of bacterial and fungal communities from the top-down control in food webs. Altogether, we provide novel evidence that fertilization significantly affects the functional groups of protistan consumers and parasites in crop-associated microbiomes, which have implications for the potential changes in their ecological functions under intensive agricultural managements.