In situ prey selection of mixotrophic and heterotrophic flagellates in Antarctic oligotrophic lakes: an analysis of the digestive vacuole content

Gerea, Marina; Queimaliños, Claudia; Schiaffino, M. Romina; Izaguirre, Irina; Forn, Irene; Massana, Ramón; Unrein, Fernando

doi:10.1093/plankt/fbs085

Journal of Plankton Research

2012

DOI: 10.1093/plankt/fbs085

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In situ prey selection of mixotrophic and heterotrophic flagellates in Antarctic oligotrophic lakes: an analysis of the digestive vacuole content

Marina Gerea

Claudia Queimaliños

M. Romina Schiaffino

et al.

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Cited by 22 publications

(21 citation statements)

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“…However, the current view is still mainly based on laboratory data, using readily growing species (12). On the other hand, a limited number of field experiments use general grazer groups rather than evaluating predation at the species level (12)(13)(14). There is a need to evaluate prey selection under natural conditions comparing flagellate species to determine more specific interactions between microbial predators and prey and assessing the relevance of selective microbial predation in the microbial loop dynamics.…”

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“…Prey identification can be addressed by techniques based on DNA fingerprinting (15,16), which allow ensuing taxonomic changes in prey assemblages (10,17). Linking prey and predator can be addressed using techniques based on fluorescence in situ hybridization (FISH), which allow detecting targeted prey inside protist food vacuoles (5,14,18,19). These techniques have been performed mostly under experimental conditions (18,20), and results suggest a high selectivity in the feeding of heterotrophic flagellates and some ciliate species investigated.…”

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“…These techniques have been performed mostly under experimental conditions (18,20), and results suggest a high selectivity in the feeding of heterotrophic flagellates and some ciliate species investigated. In contrast, the few in situ measurements showed unclear ingestion patterns for lake flagellates, and even random feeding was proposed for some bacterial groups (14). All in all, there is still limited information on the selective feeding of phagotrophic protists under natural conditions, and more remarkably, there is a huge gap of knowledge about mixotrophic flagellate species.…”

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“…CARD-FISH can be easily applied to natural assemblages to evaluate in situ prey preference of mixotrophic species and other prokaryotic grazers (14,19) using the appropriate bacterial and archaeal probes. In the present study, we examined the phagotrophic selectivity of three mixotrophic species under natural conditions.…”

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confidence: 99%

“…The phytoplankton species were identified by the size and shape of the autofluorescent plastid based on a prior taxonomic knowledge of the assemblages, which is an advantage of investigating mixotrophic flagellates at the species level with respect to the heterotrophic ones. The heterotrophic flagellates are usually grouped into operational functional groups (14,20,22). In our study, we used fluorescent probes for the domain Archaea and three groups of Eubacteria: Betaproteobacteria, Actinobacteria, and the Cytophaga-Flavobacteria group of Bacteroidetes.…”

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Some Mixotrophic Flagellate Species Selectively Graze on Archaea

Ballen-Segura

Felip

Catalan

2017

Appl Environ Microbiol

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Many phototrophic flagellates ingest prokaryotes. This mixotrophic trait becomes a critical aspect of the microbial loop in planktonic food webs because of the typical high abundance of these flagellates. Our knowledge of their selective feeding upon different groups of prokaryotes, particularly under field conditions, is still quite limited. In this study, we investigated the feeding behavior of three species (Rhodomonas sp., Cryptomonas ovata, and Dinobryon cylindricum) via their food vacuole content in field populations of a high mountain lake. We used the catalyzed reporter deposition-fluorescence in situ hybridization (CARD-FISH) protocol with probes specific for the domain Archaea and three groups of Eubacteria: Betaproteobacteria, Actinobacteria, and Cytophaga-Flavobacteria of Bacteroidetes. Our results provide field evidence that contrasting selective feeding exists between coexisting mixotrophic flagellates under the same environmental conditions and that some prokaryotic groups may be preferentially impacted by phagotrophic pressure in aquatic microbial food webs. In our study, Archaea were the preferred prey, chiefly in the case of Rhodomonas sp., which rarely fed on any other prokaryotic group. In general, prey selection did not relate to prey size among the grazed groups. However, Actinobacteria, which were clearly avoided, mostly showed a size of Ͻ0.5 m, markedly smaller than cells from the other groups.IMPORTANCE That mixotrophic flagellates are not randomly feeding in the main prokaryotic groups under field conditions is a pioneer finding in species-specific behavior that paves the way for future studies according to this new paradigm. The particular case that Archaea were preferentially affected in the situation studied shows that phagotrophic pressure cannot be disregarded when considering the distribution of this group in freshwater oligotrophic systems.KEYWORDS Archaea, mixotrophic protist, selective feeding M ixotrophic behavior, the combination of phototrophic and phagotrophic nutritional modes within a single cell, has been increasingly documented in aquatic systems (1, 2). Phagotrophy occurs in a variety of phytoplankton flagellate groups, including Chrysophyceae, dinoflagellates, prymnesiophytes, and cryptophytes, which comprise some picoeukaryotes (3-5). Currently, there is no doubt of the ubiquity of mixotrophy and its significance in the functioning of planktonic systems. Under oligotrophic conditions, phototrophic flagellates can account for up to 80% of total bacterial grazing (4,6,7).Predation by protists is among the primary mortality factors of prokaryotes in planktonic communities and thus is an important selective pressure. It becomes a structuring factor of the abundance, morphology, composition, and activity of bacterial assemblages (8, 9). The impact of protist predation appears to be modulated by the characteristics of the system (e.g., productivity) and predator and prey traits (10). Over

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Some Mixotrophic Flagellate Species Selectively Graze on Archaea

Ballen-Segura

Felip

Catalan

2017

Appl Environ Microbiol

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The Synechococcus cell surface protein SwmA increases vulnerability to predation by flagellates and ciliates

Strom

Bright

Fredrickson

et al. 2016

Limnology & Oceanography

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The genus Synechococcus, a major contributor to ocean productivity, exhibits wide genetic variability and a distinct biogeography of genetic subgroups. Synechococcus sp. strain WH8102 is a motile Sargasso Sea isolate belonging to Clade III in subcluster 5.1. Non‐flagellar motility in WH8102 depends upon two large cell surface proteins, SwmA and SwmB. In the marine plankton, Synechococcus can experience high rates of mortality from protist predators, suggesting strong selective pressure for the maintenance of anti‐predation defenses. We used knockout mutants deficient in large cell surface proteins (SwmA‐ and SwmB‐) to test the hypothesis that these proteins defend WH8102 against predation by ciliates and flagellates, important consumers of Synechococcus in aquatic ecosystems. Contrary to our hypothesis, we found that wild‐type WH8102 were preyed upon at higher rates than SwmA‐ by ciliates and by two of three tested flagellate species. Thus the SwmA protein, constitutively produced by WH8102, made this strain more rather than less vulnerable to predation. SwmA proteins link to form the S layer, a cell coating known to promote adhesion in other microbial systems, suggesting the predation vulnerability arises from increased attachment between consumers and prey. Given the SwmA‐related enhancement of predation rates, our findings suggest two possibilities for WH8102 and perhaps other Clade III Synechococcus: (1) factors other than protist predation select for production of the S layer; (2) ingestion actually increases fitness, by exposing digestion‐resistant cells to beneficial conditions in the food vacuole.

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Significance of metabolically active bacterioplankton in the frontal regions of the Northeastern Arabian Sea

et al. 2018

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In situ prey selection of mixotrophic and heterotrophic flagellates in Antarctic oligotrophic lakes: an analysis of the digestive vacuole content

Cited by 22 publications

References 72 publications

Some Mixotrophic Flagellate Species Selectively Graze on Archaea

Some Mixotrophic Flagellate Species Selectively Graze on Archaea

The Synechococcus cell surface protein SwmA increases vulnerability to predation by flagellates and ciliates

Significance of metabolically active bacterioplankton in the frontal regions of the Northeastern Arabian Sea

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