Acquired phototrophy in aquatic protists

Stoecker, Diane K.; Johnson, Matthew D.; Vargas, Colomban de; Not, Fabrice

doi:10.3354/ame01340

Cited by 293 publications

(347 citation statements)

References 285 publications

(202 reference statements)

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“…Contrary to other photosymbioses where viable symbionts can be released (37)(38)(39), Acantharia may thus enslave and exploit Phaeocystis cells over a period before either digesting them or shedding nonviable cells. Sequestration of prey organelles, such as plastids (kleptoplastidy) and nuclei (karyoklepty), is well documented (11,40), including a report that a heterotrophic dinoflagellate from Antarctic waters is capable of temporarily retaining functional Phaeocystis plastids (41). Acquisition of phototrophy in Acantharia seems rather to occur by irreversible sequestration of whole cells ("cytoklepty"), a rare biological phenomenon that has been described for the ciliate Mesodinium rubrum and the sand-dwelling flagellate Hatena arenicola that maintain cells of a cryptophyte (42) and a prasinophyte (43), respectively.…”

Section: Resultsmentioning

confidence: 99%

“…Large heterotrophic amoeboid protists, such as Radiolaria and Foraminifera from the eukaryote supergroup Rhizaria, are known to host endosymbiotic microalgae in oligotrophic oceanic surface waters (11,12). Molecular investigations associated with culturing methods have shown that symbionts can be dinoflagellates, prasinophytes, or haptophytes (13)(14)(15), but in most cases their precise identity, host specificity, and biogeography are unknown.…”

mentioning

confidence: 99%

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An original mode of symbiosis in open ocean plankton

Decelle

Probert

Bittner

et al. 2012

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

135

147

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International audienceSymbiotic relationships are widespread in nature and are fundamental for ecosystem functioning and the evolution of biodiversity. In marine environments, photosymbiosis with microalgae is best known for sustaining benthic coral reef ecosystems. Despite the importance of oceanic microbiota in global ecology and biogeochemical cycles, symbioses are poorly characterized in open ocean plankton. Here, we describe a widespread symbiotic association between Acantharia biomineralizing microorganisms that are abundant grazers in plankton communities, and members of the haptophyte genus Phaeocystis that are cosmopolitan bloom-forming microalgae. Cophylogenetic analyses demonstrate that symbiont biogeography, rather than host taxonomy, is the main determinant of the association. Molecular dating places the origin of this photosymbiosis in the Jurassic (ca. 175 Mya), a period of accentuated marine oligotrophy. Measurements of intracellular dimethylated sulfur indicate that the host likely profits from antioxidant protection provided by the symbionts as an adaptation to life in transparent oligotrophic surface waters. In contrast to terrestrial and marine symbioses characterized to date, the symbiont reported in this association is extremely abundant and ecologically active in its free-living phase. In the vast and barren open ocean, partnership with photosymbionts that have extensive free-living populations is likely an advantageous strategy for hosts that rely on such interactions. Discovery of the Acantharia-Phaeocystis association contrasts with the widely held view that symbionts are specialized organisms that are rare and ecologically passive outside the host

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

An original mode of symbiosis in open ocean plankton

Decelle

Probert

Bittner

et al. 2012

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

135

147

View full text Add to dashboard Cite

show abstract

“…At the OTU level, Spirotrichea showed different trends, before and after 2007. Spirotrichea ciliates are obligate mixotrophs, feeding on smaller prey and presumably able to use retained chlorophyte or prymnesiophytederived plastids for photosynthesis (Stoecker et al, 1988(Stoecker et al, , 2009McManus and Katz, 2009). Similar observations were reported by Jiang et al (2013) in Western Arctic Ocean where a few ciliate groups became dominant during the 2012 record ice melt, supporting the notion that microzooplankton are highly sensitive to changing physico-chemical regimes, including those associated with low-ice or freshening events.…”

Section: Interannual Microzooplankton and The Changing Arcticmentioning

confidence: 99%

Seasonal and Interannual Changes in Ciliate and Dinoflagellate Species Assemblages in the Arctic Ocean (Amundsen Gulf, Beaufort Sea, Canada)

et al. 2017

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Recent studies have focused on how climate change could drive changes in phytoplankton communities in the Arctic. In contrast, ciliates and dinoflagellates that can contribute substantially to the mortality of phytoplankton have received less attention. Some dinoflagellate and ciliate species can also contribute to net photosynthesis, which suggests that species composition could reflect food web complexity. To identify potential seasonal and annual species occurrence patterns and to link species with environmental conditions, we first examined the seasonal pattern of microzooplankton and then performed an in-depth analysis of interannual species variability. We used high-throughput amplicon sequencing to identify ciliates and dinoflagellates to the lowest taxonomic level using a curated Arctic 18S rRNA gene database. DNA-and RNA-derived reads were generated from samples collected from the Canadian Arctic from November 2007 to July 2008. The proportion of ciliate reads increased in the surface toward summer, when salinity was lower and smaller phytoplankton prey were abundant, while chloroplastidic dinoflagellate species increased at the subsurface chlorophyll maxima (SCM), where inorganic nutrient concentrations were higher. Comparing communities collected in summer and fall from 2003 to 2010, we found that microzooplankton community composition change was associated with the record ice minimum in the summer of 2007. Specifically, reads from smaller predatory species like Laboea, Monodinium, and Strombidium and several unclassified ciliates increased in the summer after 2007, while the other usually summer-dominant dinoflagellate taxa decreased. The ability to exploit smaller prey, which are predicted to dominate the future Arctic, could be an advantage for these smaller ciliates in the wake of the changing climate.

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“…In the evolution of these protists, phagotrophy is the ancestral state and phototrophy is the derived, more recent, state (Raven et al, 2009). This evolutionary pathway, which is neither fixed nor irreversible, has included a multitude of events associated with acquisition of structures and of symbionts that have led to the evolution of organelles including plastids and other characteristics (de Castro et al, 2009;Stoecker et al, 2009). "Strict" phototrophy and "strict" phagotrophy thus form the two extreme ends of a spectrum, with most protist groups in the photic zone functionally occupying the intermediate niche zone as mixotrophs.…”

mentioning

confidence: 99%

“…Mixotrophy is not displayed by any unique taxonomic group but, rather, occurs amongst different species ranging over a variety of groups (Stoecker et al, 2009;. It is a common phenomenon occurring widely in marine (e.g.…”

mentioning

confidence: 99%

The role of mixotrophic protists in the biological carbon pump

et al. 2014

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Abstract. The traditional view of the planktonic food web describes consumption of inorganic nutrients by photoautotrophic phytoplankton, which in turn supports zooplankton and ultimately higher trophic levels. Pathways centred on bacteria provide mechanisms for nutrient recycling. This structure lies at the foundation of most models used to explore biogeochemical cycling, functioning of the biological pump, and the impact of climate change on these processes. We suggest an alternative new paradigm, which sees the bulk of the base of this food web supported by protist plankton communities that are mixotrophic -combining phototrophy and phagotrophy within a single cell. The photoautotrophic eukaryotic plankton and their heterotrophic microzooplankton grazers dominate only during the developmental phases of ecosystems (e.g. spring bloom in temperate systems). With their flexible nutrition, mixotrophic protists dominate in more-mature systems (e.g. temperate summer, established eutrophic systems and oligotrophic systems); the more-stable water columns suggested under climate change may also be expected to favour these mixotrophs. We explore how such a predominantly mixotrophic structure affects microbial trophic dynamics and the biological pump. The mixotroph-dominated structure differs fundamentally in its flow of energy and nutrients, with a shortened and potentially more efficient chain from nutrient regeneration to primary production. Furthermore, mixotrophy enables a direct conduit for the support of primary production from bacterial production. We show how the exclusion of an explicit mixotrophic component in studies of the pelagic microbial communities leads to a failure to capture the true dynamics of the carbon flow. In order to prevent a misinterpretation of the full implications of climate change upon biogeochemical cycling and the functioning of the biological pump, we recommend inclusion of multi-nutrient mixotroph models within ecosystem studies.

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Acquired phototrophy in aquatic protists

Cited by 293 publications

References 285 publications

An original mode of symbiosis in open ocean plankton

An original mode of symbiosis in open ocean plankton

Seasonal and Interannual Changes in Ciliate and Dinoflagellate Species Assemblages in the Arctic Ocean (Amundsen Gulf, Beaufort Sea, Canada)

The role of mixotrophic protists in the biological carbon pump

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