<i>In situ</i> interactions between photosynthetic picoeukaryotes and bacterioplankton in the <scp>A</scp>tlantic <scp>O</scp>cean: evidence for mixotrophy

Hartmann, Manuela; Zubkov, Mikhail V.; Scanlan, David J.; Lepère, Cécile

doi:10.1111/1758-2229.12084

Cited by 71 publications

(73 citation statements)

References 31 publications

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“…Despite this growing understanding of the diversity and the key roles that PPE have as primary producers and grazers of prokaryotes in marine waters, many of the major clades remain uncultured (Vaulot et al, 2008;Massana, 2011). Consequently, there is relatively little information on their morphology and physiology that could aid in understanding environmental conditions that affect their growth and relative abundances (DuRand et al, 2002;Foulon et al, 2008;Hartmann et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…A temperate strain identified as M. pusilla was previously shown to be bacterivorous (González et al, 1993), but there still is little eco-physiological information available for any of the clades (Foulon et al, 2008;Hartmann et al, 2013). To this end, we compared the effect of light and nutrients on rates of bacterivory for Micromonas CCMP2099, tested its ability to discriminate between prey sizes and examined autotrophic functioning (P vs I) in different light and nutrient conditions.…”

Section: Introductionmentioning

confidence: 99%

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Phagotrophy by the picoeukaryotic green alga Micromonas: implications for Arctic Oceans

2014

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Photosynthetic picoeukaryotes (PPE) are recognized as major primary producers and contributors to phytoplankton biomass in oceanic and coastal environments. Molecular surveys indicate a large phylogenetic diversity in the picoeukaryotes, with members of the Prymnesiophyceae and Chrysophyseae tending to be more common in open ocean waters and Prasinophyceae dominating coastal and Arctic waters. In addition to their role as primary producers, PPE have been identified in several studies as mixotrophic and major predators of prokaryotes. Mixotrophy, the combination of photosynthesis and phagotrophy in a single organism, is well established for most photosynthetic lineages. However, green algae, including prasinophytes, were widely considered as a purely photosynthetic group. The prasinophyte Micromonas is perhaps the most common picoeukaryote in coastal and Arctic waters and is one of the relatively few cultured representatives of the picoeukaryotes available for physiological investigations. In this study, we demonstrate phagotrophy by a strain of Micromonas (CCMP2099) isolated from Arctic waters and show that environmental factors (light and nutrient concentration) affect ingestion rates in this mixotroph. In addition, we show size-selective feeding with a preference for smaller particles, and determine P vs I (photosynthesis vs irradiance) responses in different nutrient conditions. If other strains have mixotrophic abilities similar to Micromonas CCMP2099, the widespread distribution and frequently high abundances of Micromonas suggest that these green algae may have significant impact on prokaryote populations in several oceanic regimes.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Phagotrophy by the picoeukaryotic green alga Micromonas: implications for Arctic Oceans

2014

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“…1A). The consistency of the phase and period of the oscillations in the rates of cell mortality was particularly surprising across such a large spatial scale given the diversity of potential sources of Prochlorococcus mortality (e.g., viruses and grazers) (21,22). A similar diel pattern of cell production and cell mortality was observed in the same region the previous year (November 2010; SI Appendix, Fig.…”

Section: Significancementioning

confidence: 83%

“…There is growing evidence that viral infection rates in the cyanobacteria Synechococcus and other marine phytoplankton depend on light either directly or indirectly via the host's cell cycle (25,26). Mixotrophic protists, such as crysophytes, can graze at night and photosynthesize during the day (27), some of which consume Prochlorococcus in oligotrophic regions (22). Modeled cell mortality emulates our observations if we assume that the per-capita rate of viral infection varies over the day/night cycle or that grazing only occurs at night (Fig.…”

Section: Phytoplankton (Simentioning

confidence: 99%

Light-driven synchrony of Prochlorococcus growth and mortality in the subtropical Pacific gyre

Ribalet

Swalwell

Clayton

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

127

156

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Theoretical studies predict that competition for limited resources reduces biodiversity to the point of ecological instability, whereas strong predator/prey interactions enhance the number of coexisting species and limit fluctuations in abundances. In open ocean ecosystems, competition for low availability of essential nutrients results in relatively few abundant microbial species. The remarkable stability in overall cell abundance of the dominant photosynthetic cyanobacterium Prochlorococcus is assumed to reflect a simple food web structure strongly controlled by grazers and/or viruses. This hypothesized link between stability and ecological interactions, however, has been difficult to test with open ocean microbes because sampling methods commonly have poor temporal and spatial resolution. Here we use continuous techniques on two different winter-time cruises to show that Prochlorococcus cell production and mortality rates are tightly synchronized to the day/night cycle across the subtropical Pacific Ocean. In warmer waters, we observed harmonic oscillations in cell production and mortality rates, with a peak in mortality rate consistently occurring ∼6 h after the peak in cell production. Essentially no cell mortality was observed during daylight. Our results are best explained as a synchronized two-component trophic interaction with the per-capita rates of Prochlorococcus consumption driven either directly by the day/night cycle or indirectly by Prochlorococcus cell production. Light-driven synchrony of food web dynamics in which most of the newly produced Prochlorococcus cells are consumed each night likely enforces ecosystem stability across vast expanses of the open ocean.cyanobacteria | cell division | mortality | flow cytometry | SeaFlow P otential interdependencies between species diversity and ecosystem stability have gained increased focus due to global changes in species distributions and abundances (1). Strong predator-prey interactions are predicted to enhance the number of coexisting species and limit fluctuations in abundances (2, 3), whereas competition for limited resources is predicted to reduce biodiversity, in some instances, to the point of ecological instability (3, 4). Mechanisms underlying ecosystem stability remain challenging to characterize on relevant temporal and spatial scales, in part because few empirical data are available to test these theories.Our focus is on the microbial communities within surface waters of the vast oligotrophic gyre of the north Pacific Subtropical Ocean. Here, competition for low concentrations of essential nutrients is hypothesized to result in relatively few abundant microbial species, typified by their extremely small cell sizes and streamlined genomes (5). The cyanobacterium Prochlorococcus numerically dominates the photosynthetic community in these regions, with a relatively constant cell abundance close to half a billion cells per liter despite a population doubling time of approximately one day (6). Such constant cell numbers are predicted when both...

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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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confidence: 99%

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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In situ interactions between photosynthetic picoeukaryotes and bacterioplankton in the Atlantic Ocean: evidence for mixotrophy

Cited by 71 publications

References 31 publications

Phagotrophy by the picoeukaryotic green alga Micromonas: implications for Arctic Oceans

Phagotrophy by the picoeukaryotic green alga Micromonas: implications for Arctic Oceans

Light-driven synchrony of Prochlorococcus growth and mortality in the subtropical Pacific gyre

Some Mixotrophic Flagellate Species Selectively Graze on Archaea

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