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Oceanic protists with different forms of acquired phototrophy display contrasting biogeographies and abundance - PubMed

  • ️Sun Jan 01 2017

. 2017 Aug 16;284(1860):20170664.

doi: 10.1098/rspb.2017.0664.

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Oceanic protists with different forms of acquired phototrophy display contrasting biogeographies and abundance

S G Leles et al. Proc Biol Sci. 2017.

Abstract

This first comprehensive analysis of the global biogeography of marine protistan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitutive capacity for photosynthesis (i.e. non-constitutive mixotrophs, NCMs), acquire their phototrophic potential through either integration of prey-plastids or through endosymbiotic associations with photosynthetic microbes. Analysis of field data reveals that 40-60% of plankton traditionally labelled as (non-phototrophic) microzooplankton are actually NCMs, employing acquired phototrophy in addition to phagotrophy. Specialist NCMs acquire chloroplasts or endosymbionts from specific prey, while generalist NCMs obtain chloroplasts from a variety of prey. These contrasting functional types of NCMs exhibit distinct seasonal and spatial global distribution patterns. Mixotrophs reliant on 'stolen' chloroplasts, controlled by prey diversity and abundance, dominate in high-biomass areas. Mixotrophs harbouring intact symbionts are present in all waters and dominate particularly in oligotrophic open ocean systems. The contrasting temporal and spatial patterns of distribution of different mixotroph functional types across the oceanic provinces, as revealed in this study, challenges traditional interpretations of marine food web structures. Mixotrophs with acquired phototrophy (NCMs) warrant greater recognition in marine research.

Keywords: acquired phototrophy; biogeography; kleptoplasty; marine protists; mixotrophy; photosymbiosis.

© 2017 The Author(s).

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Conflict of interest statement

We have no competing interests.

Figures

Figure 1.
Figure 1.

Global distribution of protists with acquired phototrophy (non-constitutive mixotrophs, NCMs). Functional groups identify protists which acquire plastids from a variety of prey (generalist NCMs, GNCMs; blue (a)), from specific prey (plastidic specialist NCMs, pSNCMs; red (b)), or enslave entire specific autotrophic prey as symbionts (endosymbiotic SNCMs, eSNCMs; green (c)). Images next to each map provide protist genus examples within each functional group. From left to right (size as length): (a) GNCMs Laboea (100 µm) and Strombidium (50 µm); (b) pSNCMs, Mesodinium (60 µm) and Dinophysis (40 µm); (c) eSNCMs, Sphaerozoum (200 µm) and Noctiluca (500 µm). On maps, symbols correspond to the exact location where mixotrophic species/taxa were found (from more than 110 000 records); the grid indicates biogeographic provinces. Colour-cast provinces indicate the presence of NCMs and white provinces correspond to the absence. Provinces marked with asterisks indicate that studies conducted in these areas did not record the presence of mixotrophic species; unmarked white provinces indicate a lack of field studies providing information on acquired phototrophy among microzooplankton.

Figure 2.
Figure 2.

Differences in the biogeography of non-constitutive mixotrophs (NCMs). (a) Results from the NMDS analysis showing the ordination of species and biomes in a two-dimensional space. Species were classified according to the non-constitutive mixotroph functional groups (GNCMs, pSNCMs and eSNCMs). Each symbol represents an NCM species; different symbols and dashed ellipses (at 80% CI) represent different functional groups. The different biomes are: MS, Mediterranean Sea; PS, Polar Seas; TS, Temperate Seas; CS, Coastal Seas; OG, Oligotrophic Gyres; CU, Coastal Upwelling; EU, Equatorial Upwelling (see also the electronic supplementary material, figure S3). (b,c) Relative contribution of mixotrophs (% biomass) as a function of (b) nutrient load and (c) system variability. Contribution of mixotrophic ciliate biomass (GNCMs + the pSNCM Mesodinium; purple) is plotted relative to total ciliate biomass while contribution of mixotrophic Rhizarian biomass (green) is presented relative to total Rhizarian biomass. Annual average and variance of net primary productivity (NPP) were used as a proxy for nutrient load and system variability, respectively (data obtained from [17]); each symbol represents a biogeographic province (see also the electronic supplementary material). Loess regressions were fitted to data using R package ggplot2; 95% CIs shown.

Figure 3.
Figure 3.

Spatial and temporal distribution of protists with acquired phototrophy. (a) GNCM ciliates, (b) pSNCM Mesodinium spp., (c) eSNCM Rhizaria. Seasonal biomass abundance for each group is shown across different biomes (note that biomass units in (a,b) are different from (c)); n indicates the total number of observations used. No published data were available for the Coastal Upwelling biome.

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