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

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.

[1]  F. Not,et al.  Mixotrophy everywhere on land and in water: the grand écart hypothesis. , 2017, Ecology letters.

[2]  D. Caron,et al.  Mixotrophy in the Marine Plankton. , 2017, Annual review of marine science.

[3]  N. Mayot,et al.  In situ imaging reveals the biomass of giant protists in the global ocean , 2016, Nature.

[4]  C. Gobler,et al.  The contribution of inorganic and organic nutrients to the growth of a North American isolate of the mixotrophic dinoflagellate, Dinophysis acuminata , 2015 .

[5]  P. Bork,et al.  Eukaryotic plankton diversity in the sunlit ocean , 2015, Science.

[6]  R. Majchrowski,et al.  Latitudinal pattern of abundance and composition of ciliate communities in the surface waters of the Atlantic Ocean , 2014 .

[7]  F. G. Figueiras,et al.  Estimating phytoplankton size-fractionated primary production in the northwestern Iberian upwelling: Is mixotrophy relevant in pigmented nanoplankton? , 2014 .

[8]  Jialin Liu,et al.  Mechanisms of Microbial Carbon Sequestration in the Ocean - Future Research Directions , 2014 .

[9]  Sushma G. Parab,et al.  Massive outbreaks of Noctiluca scintillans blooms in the Arabian Sea due to spread of hypoxia , 2014, Nature Communications.

[10]  L. Mafra,et al.  Diarrheic toxins in field-sampled and cultivated Dinophysis spp. cells from southern Brazil , 2014, Journal of Applied Phycology.

[11]  J. Burkholder,et al.  The role of mixotrophic protists in the biological carbon pump , 2013 .

[12]  Matthew D. Johnson,et al.  Acquired phototrophy in Mesodinium and Dinophysis – A review of cellular organization, prey selectivity, nutrient uptake and bioenergetics , 2013 .

[13]  D. W. Coats,et al.  DINOPHYSIS CAUDATA (DINOPHYCEAE) SEQUESTERS AND RETAINS PLASTIDS FROM THE MIXOTROPHIC CILIATE PREY MESODINIUM RUBRUM 1 , 2012, Journal of phycology.

[14]  Manuela Hartmann,et al.  Mixotrophic basis of Atlantic oligotrophic ecosystems , 2012, Proceedings of the National Academy of Sciences.

[15]  D. Kirchman Processes in Microbial Ecology , 2012, Oxford Scholarship Online.

[16]  Lee Ann McCue,et al.  Red Waters of Myrionecta rubra are Biogeochemical Hotspots for the Columbia River Estuary with Impacts on Primary/Secondary Productions and Nutrient Cycles , 2012, Estuaries and Coasts.

[17]  B. Reguera,et al.  Harmful Dinophysis species: A review , 2012 .

[18]  A. Al-Azri,et al.  Geographical distribution of red and green Noctiluca scintillans , 2011 .

[19]  G. Hansen,et al.  Spatial distribution of symbiont-bearing dinoflagellates in the Indian Ocean in relation to oceanographic regimes , 2010 .

[20]  Josette Garnier,et al.  Anthropogenic perturbations of the silicon cycle at the global scale: Key role of the land‐ocean transition , 2009 .

[21]  Matthew D. Johnson,et al.  Acquired phototrophy in aquatic protists , 2009 .

[22]  I. Salter,et al.  Radiolaria: Major exporters of organic carbon to the deep ocean , 2009 .

[23]  Patricia M. Glibert,et al.  Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters , 2008 .

[24]  Glen A. Tarran,et al.  High bacterivory by the smallest phytoplankton in the North Atlantic Ocean , 2008, Nature.

[25]  N. Okamoto,et al.  A Secondary Symbiosis in Progress? , 2005, Science.

[26]  J. Dolan,et al.  Costs, benefits and characteristics of mixotrophy in marine oligotrichs , 2000 .

[27]  J. Randerson,et al.  Primary production of the biosphere: integrating terrestrial and oceanic components , 1998, Science.

[28]  A. Longhurst Ecological Geography of the Sea , 1998 .

[29]  D. Stoecker,et al.  Micro- and mesoprotozooplankton at 140*W in the equatorial Pacific: heterotrophs and mixotrophs , 1996 .

[30]  F. H. Chang Quantitative distribution of microzooplankton off Westland, New Zealand , 1990 .

[31]  D. Caron,et al.  Defining Planktonic Protist Functional Groups on Mechanisms for Energy and Nutrient Acquisition: Incorporation of Diverse Mixotrophic Strategies. , 2016, Protist.

[32]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[33]  J. Burkholder,et al.  Misuse of the phytoplankton-zooplankton dichotomy : the need to assign organisms as mixotrophs within plankton functional types , 2013 .

[34]  Matthew D. Johnson The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles , 2010, Photosynthesis Research.

[35]  A. Longhurst TOWARD AN ECOLOGICAL GEOGRAPHY OF THE SEA , 2007 .