Constant abundances of ubiquitous uncultured protists in the open sea assessed by automated microscopy

Mangot, Jean‐François; Forn, Irene; Obiol, Aleix; Massana, Ramón

doi:10.1111/1462-2920.14408

Cited by 18 publications

(18 citation statements)

References 75 publications

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“…Actually, most associations were not considered as they were either weak (low correlation) or they just represented similar or different environmental preference (mainly temperature) between MAST-4 and bacterial OTUs. Altogether, this suggests that MAST-4 abundance and occurrence is weakly coupled to bacterial distributions and abundance in the upper ocean, which agrees with previous studies where temperature appeared as the main driver of heterotrophic flagellates abundances (42). We detected a substantial number of taxa that were positively associated to either MAST-4B/C or MAST-4A but not to both.…”

Section: Discussionsupporting

confidence: 91%

Evolutionary diversification of tiny ocean predators

Latorre¹,

Deutschmann²,

Labarre³

et al. 2020

Preprint

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Unicellular eukaryotic predators have a crucial role in the functioning of the ocean ecosystem by recycling nutrients and energy that are channeled to upper trophic levels. Traditionally, these evolutionary-diverse organisms have been combined into a single functional group (Heterotrophic flagellates), overlooking their organismal differences. Here we investigate four evolutionary related species belonging to one cosmopolitan family of uncultured marine picoeukaryotic predators: MAST-4 (species A, B, C, and E). Co-occurrence and distribution analyses in the global surface ocean indicated contrasting patterns in MAST-4A & C, suggesting adaptation to different temperatures. We then investigated whether these spatial distribution patterns were mirrored by MAST-4 genomic content using Single-Cell Genomics. Analyses of 69 single-cells recovered 66-83% of the MAST-4A/B/C/E genomes, which displayed substantial inter-species divergence. MAST-4 genomes were similar in terms of broad gene functional categories, but they differed in enzymes of ecological relevance, such as glycoside hydrolases (GHs), which are part of the food degradation machinery in MAST-4. Interestingly, MAST-4 species featuring a similar GH composition co-excluded each other (A & C) in the surface global ocean, while species with a different set of GHs appeared to be able to co-exist (species B & C) suggesting further niche diversification associated to prey digestion. We propose that differential niche adaptation to temperature and prey type has promoted adaptive evolutionary diversification in MAST-4. Altogether, we show that minute ocean predators from the same family may have different biogeography and genomic content, which need to be accounted to better comprehend marine food webs.

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Section: Discussionsupporting

confidence: 91%

Evolutionary diversification of tiny ocean predators

Latorre¹,

Deutschmann²,

Labarre³

et al. 2020

Preprint

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“…For instance, the genus Paraphysomonas was found to contribute below 1% to the total abundance of HF (Lim et al, 1999). In contrast, novel lineages of marine Stramenopiles (MAST), especially nanoplanktonic MAST-1 (cell size: 4-7 µm) and picoplanktonic MAST-4 (cell size: 2-3 µm), turned out to be ubiquitous in open oceans, contributing together to about 20% of all HF (Massana et al, 2006b;Mangot et al, 2018), and exhibiting growth rates between 0.4 and 0.8 per day (Massana et al, 2006a). Two morphotypes of the MAST-6 lineage were observed in the brackish Baltic Sea: larger (approximately 15 µm, Figure 4E) that formed a conspicuous peak when the salinity dropped to 6.2, and smaller (around 6 µm, Figure 6F) that dominated at salinities > 7 (Piwosz and Pernthaler, 2010).…”

Section: Novel Hf and Mf In Marine Environmentsmentioning

confidence: 99%

“…Alternatively, percent proportion of counted cells hybridized with a specific probe can be plotted against the number of counted DNA-stained cells until the plateau is reached, indicating the sufficient counting effort. Flow cytometry or automatic image acquisition microscopy may allow for statistically robust abundance estimates of rare lineages (Simon et al, 1995;Biegala et al, 2003;Mangot et al, 2018).…”

Section: Card-fish Basicsmentioning

confidence: 99%

CARD-FISH in the Sequencing Era: Opening a New Universe of Protistan Ecology

et al. 2021

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Phagotrophic protists are key players in aquatic food webs. Although sequencing-based studies have revealed their enormous diversity, ecological information on in situ abundance, feeding modes, grazing preferences, and growth rates of specific lineages can be reliably obtained only using microscopy-based molecular methods, such as Catalyzed Reporter Deposition-Fluorescence in situ Hybridization (CARD-FISH). CARD-FISH is commonly applied to study prokaryotes, but less so to microbial eukaryotes. Application of this technique revealed that Paraphysomonas or Spumella-like chrysophytes, considered to be among the most prominent members of protistan communities in pelagic environments, are omnipresent but actually less abundant than expected, in contrast to little known groups such as heterotrophic cryptophyte lineages (e.g., CRY1), cercozoans, katablepharids, or the MAST lineages. Combination of CARD-FISH with tracer techniques and application of double CARD-FISH allow visualization of food vacuole contents of specific flagellate groups, thus considerably challenging our current, simplistic view that they are predominantly bacterivores. Experimental manipulations with natural communities revealed that larger flagellates are actually omnivores ingesting both prokaryotes and other protists. These new findings justify our proposition of an updated model of microbial food webs in pelagic environments, reflecting more authentically the complex trophic interactions and specific roles of flagellated protists, with inclusion of at least two additional trophic levels in the nanoplankton size fraction. Moreover, we provide a detailed CARD-FISH protocol for protists, exemplified on mixo- and heterotrophic nanoplanktonic flagellates, together with tips on probe design, a troubleshooting guide addressing most frequent obstacles, and an exhaustive list of published probes targeting protists.

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“…The ability of heterotrophic protists to utilize DIN reveals an additional pathway within the microbial loop for N-assimilation into the food web. Heterotrophic protists are ubiquitous (Pernice et al, 2015;Mangot et al, 2018) and their functionality diverse (Sherr et al, 2007;Caron et al, 2012;Mitra et al, 2016). Many phototrophic species contribute to primary production and inorganic nutrient uptake, whilst others like Ammonia sp.…”

Section: The Marine Nitrogen Cyclementioning

confidence: 99%

Heterotrophic Foraminifera Capable of Inorganic Nitrogen Assimilation

et al. 2020

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Nitrogen availability often limits biological productivity in marine systems, where inorganic nitrogen, such as ammonium is assimilated into the food web by bacteria and photoautotrophic eukaryotes. Recently, ammonium assimilation was observed in kleptoplast-containing protists of the phylum foraminifera, possibly via the glutamine synthetase/glutamate synthase (GS/GOGAT) assimilation pathway imported with the kleptoplasts. However, it is not known if the ubiquitous and diverse heterotrophic protists have an innate ability for ammonium assimilation. Using stable isotope incubations (15N-ammonium and 13C-bicarbonate) and combining transmission electron microscopy (TEM) with quantitative nanoscale secondary ion mass spectrometry (NanoSIMS) imaging, we investigated the uptake and assimilation of dissolved inorganic ammonium by two heterotrophic foraminifera; a non-kleptoplastic benthic species, Ammonia sp., and a planktonic species, Globigerina bulloides. These species are heterotrophic and not capable of photosynthesis. Accordingly, they did not assimilate 13C-bicarbonate. However, both species assimilated dissolved 15N-ammonium and incorporated it into organelles of direct importance for ontogenetic growth and development of the cell. These observations demonstrate that at least some heterotrophic protists have an innate cellular mechanism for inorganic ammonium assimilation, highlighting a newly discovered pathway for dissolved inorganic nitrogen (DIN) assimilation within the marine microbial loop.

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Constant abundances of ubiquitous uncultured protists in the open sea assessed by automated microscopy

Cited by 18 publications

References 75 publications

Evolutionary diversification of tiny ocean predators

Evolutionary diversification of tiny ocean predators

CARD-FISH in the Sequencing Era: Opening a New Universe of Protistan Ecology

Heterotrophic Foraminifera Capable of Inorganic Nitrogen Assimilation

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