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Mixotrophic Protists Display Contrasted Biogeographies in the Global Ocean

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Mixotrophic Protists Display Contrasted Biogeographies in the Global Ocean The ISME Journal (2019) 13:1072–1083 https://doi.org/10.1038/s41396-018-0340-5 ARTICLE Mixotrophic protists display contrasted biogeographies in the global ocean 1,2 3 2 4 2 1,2 Emile Faure ● Fabrice Not ● Anne-Sophie Benoiston ● Karine Labadie ● Lucie Bittner ● Sakina-Dorothée Ayata Received: 2 July 2018 / Revised: 13 December 2018 / Accepted: 13 December 2018 / Published online: 14 January 2019 © International Society for Microbial Ecology 2019 Abstract Mixotrophy, or the ability to acquire carbon from both auto- and heterotrophy, is a widespread ecological trait in marine protists. Using a metabarcoding dataset of marine plankton from the global ocean, 318,054 mixotrophic metabarcodes represented by 89,951,866 sequences and belonging to 133 taxonomic lineages were identified and classified into four mixotrophic functional types: constitutive mixotrophs (CM), generalist non-constitutive mixotrophs (GNCM), endo-symbiotic specialist non-constitutive mixotrophs (eSNCM), and plastidic specialist non-constitutive mixotrophs (pSNCM). Mixotrophy appeared ubiquitous, and the distributions of the four mixotypes were analyzed to identify the abiotic factors shaping their biogeographies. Kleptoplastidic mixotrophs (GNCM and pSNCM) were detected in new zones compared to previous 1234567890();,: 1234567890();,: morphological studies. Constitutive and non-constitutive mixotrophs had similar ranges of distributions. Most lineages were evenly found in the samples, yet some of them displayed strongly contrasted distributions, both across and within mixotypes. Particularly divergent biogeographies were found within endo-symbiotic mixotrophs, depending on the ability to form colonies or the mode of symbiosis. We showed how metabarcoding can be used in a complementary way with previous morphological observations to study the biogeography of mixotrophic protists and to identify key drivers of their biogeography. Introduction taxonomic and functional diversity that remains hard to define [2, 3]. This variety of organisms is having an impact Marine unicellular eukaryotes, or protists, have a tre- on major biogeochemical cycles such as carbon, oxygen, mendous range of life styles, sizes and forms [1], showing a nitrogen, sulfur, silica, or iron, while being at the base of marine trophic networks [4–8]. Hence, they are key actors of the global functioning of the ocean. These authors contributed equally: Lucie Bittner, Sakina-Dorothée Historically, marine protists have been classified into two Ayata groups depending on their trophic strategy: the photo- Supplementary information The online version of this article (https:// synthetic plankton (phytoplankton) and the heterotrophic doi.org/10.1038/s41396-018-0340-5) contains supplementary plankton (zooplankton). It is now clear that mixotrophy, i.e., material, which is available to authorized users. the ability to combine autotrophy and heterotrophy, has been largely underestimated and is commonly found in * Emile Faure [email protected] planktonic protists [6, 9–13]. Instead of a dichotomy between two trophic types, their trophic regime should be 1 Sorbonne Université, CNRS, Laboratoire d’océanographie de regarded as a continuum between full phototrophy and full Villefranche, LOV, 06230 Villefranche-sur-Mer, France heterotrophy, with species from many planktonic lineages 2 Institut de Systématique, Evolution, Biodiversité (ISYEB), lying between these two extremes [10]. Mitra et al. [11] ’ Muséum national d Histoire naturelle, CNRS, Sorbonne have proposed a classification of marine mixotrophic pro- Université, EPHE, CP 50, 57 rue Cuvier, 75005 Paris, France tists into four functional groups, or mixotypes. The con- 3 Sorbonne Université, CNRS, UMR7144 Adaptation and Diversity stitutive mixotrophs, or CM, are photosynthetic organisms in Marine Environment (AD2M) Laboratory, Ecology of Marine “ Plankton team, Station Biologique de Roscoff, Place Georges that are capable of phagotrophy, also called phytoplankton Teissier, 29680 Roscoff, France that eat” [11]. They include most mixotrophic nano- fl 4 Genoscope, Institut de biologie François-Jacob, Commissariat à agellates (e.g., Prymnesium parvum, Karlodinium l’Energie Atomique (CEA), Evry, France, 91057 Evry, France micrum). On the opposite, the non-constitutive mixotrophs, Mixotrophic protists display contrasted biogeographies in the global ocean 1073 or “photosynthetic zooplankton”, are heterotrophic organ- We tested (i) if new information on marine mixotrophic isms that have developed the ability to acquire energy protists distribution can be gained in comparison with pre- through photosynthesis [9]. This ability can be acquired in vious morphological identifications [27]; (ii) if the con- three different ways: the generalist non-constitutive mixo- stitutive mixotrophs, which are not addressed in Leles et al. trophs (GNCM) steal the chloroplasts of their prey, such as [27], and the non-constitutive mixotrophs diverge in terms most plastid-retaining oligotrich ciliates (e.g., Laboea of biogeography; (iii) if the study of diversity and abun- strobila), the plastidic specialist non-constitutive mixo- dance of environmental metabarcodes could lead to the trophs (pSNCM) steal the chloroplasts of a specific type of definition of key environmental factors shaping mixotrophic prey (e.g., Mesodinium rubrum or Dinophysis spp.), and communities. finally the endo-symbiotic specialist non-constitutive mix- otrophs (eSNCM) are bearing photosynthetically active endo-symbionts (most mixotrophic Rhizaria from Collo- Materials and methods daria, Acantharea, Polycystinea, and Foraminifera, as well as dinoflagellates like Noctiluca scintillans). Samples collection and dataset creation As drivers of biogeochemical cycles in the global ocean, and particularly of the biological carbon pump [5, 14, 15], Metabarcoding datasets from the worldwide Tara Oceans marine protists are a key part of ocean biogeochemical sampling campaigns that took place between 2009 and 2013 models [7, 16–18]. However, physiological details of mix- [31, 33] (data published in open access at the European otrophic energy acquisition strategies have only been stu- Nucleotide Archive under project accession number died in a restricted number of lineages [9, 19, 20]. They PRJEB6610) were investigated. We analyzed 659 samples appear to be quite complex and greatly differ across mix- from 122 distinct stations, and for each sample, the V9-18S otypes, which makes mixotrophy hard to include in a simple ribosomal DNA region was sequenced through Illumina model structure [21–25]. Hence at this time, mixotrophy is HiSeq [32]. Assembled and filtered V9 metabarcodes (cf. not included in most biogeochemical models, neglecting the details in de Vargas et al. [2]) were assigned to the lowest amount of carbon fixed by non-constitutive mixotrophs taxonomic rank possible via the Protist Ribosomal Reference through photosynthesis, and missing the population (PR2) database [34]. To limit false positives, we chose to only dynamics of photosynthetically active constitutive mixo- analyze the metabarcodes (i.e., unique versions of trophs that can still grow under nutrient limitation [23, 26]. V9 sequences) for which the assignment to a reference This is most probably skewing climatic models predictions sequence had been achieved with a similarity of 95% or [11, 26], as well as our ability to understand and prevent higher. This represents 65% of the total dataset in terms of future effects of global change. metabarcodes and 84% in terms of total sequences. Our A better understanding of the environmental diversity of dataset involved 1,492,912,215 sequences, distributed into marine mixotrophic protists, as well as a description of the 4,099,567 metabarcodes assigned to 5071 different taxonomic abiotic factors driving their biogeography at global scale are assignations, going from species to kingdom level precision. still needed, in particular to integrate them in biogeo- chemical models. Leles et al. [27] attempted to tackle this Defining a set of mixotrophic organisms problem by reviewing about 110,000 morphological iden- tification records of a set of more than 60 mixotrophic Among these 5071 taxonomic assignations, we searched for protists species in the ocean, taken from the Ocean Bio- mixotrophic protist lineages, taking into account the four geographic Information System (OBIS) database. They mixotypes described by Mitra et al. [11]: constitutive mix- found distinctive patterns in the biogeography of the three otrophs (CM), generalist non-constitutive mixotrophs different non-constitutive mixotypes (GNCM, pSNCM, and (GNCM), endo-symbiotic specialist non-constitutive mixo- eSNCM), highlighting the need to better understand such trophs (eSNCM), and plastidic specialist non-constitutive diverging distributions [27]. Environmental molecular bio- mixotrophs (pSNCM). We used the table S2 from Leles diversity surveys through metabarcoding have been widely et al. [27], which is referencing 71 species or genera used in the past fifteen years to decipher planktonic taxo- belonging to three non-constitutive mixotypes (GNCM, nomic diversity [2, 28–30]. Here, we exploited the global pSNCM, and eSNCM), as well as multiple other sources Tara Oceans datasets [31–33], and identified 133 mixo- coming from the recent literature on mixotrophy [6, 9–12, trophic lineages, that we classified into the four mixotypes 35–47], and inputs from mixotrophic protists’ taxonomy defined by Mitra et al. [11]. This first ever set of mixo- specialists (cf. Acknowledgments
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