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

S G Leles; A Mitra; K J Flynn; D K Stoecker; P J Hansen; A Calbet; G B McManus; R W Sanders; D A Caron; F Not; G M Hallegraeff; P Pitta; J A Raven; M D Johnson; P M Glibert; S Våge

doi:10.1098/rspb.2017.0664

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

Proc Biol Sci. 2017 Aug 16;284(1860):20170664. doi: 10.1098/rspb.2017.0664.

Authors

S G Leles¹, A Mitra², K J Flynn¹, D K Stoecker³, P J Hansen⁴, A Calbet⁵, G B McManus⁶, R W Sanders⁷, D A Caron⁸, F Not⁹, G M Hallegraeff¹⁰, P Pitta¹¹, J A Raven^{12

13}, M D Johnson¹⁴, P M Glibert³, S Våge¹⁵

Affiliations

¹ Biosciences, Swansea University, Singleton Park, Swansea SA2 8PP, UK.
² Biosciences, Swansea University, Singleton Park, Swansea SA2 8PP, UK a.mitra@swansea.ac.uk.
³ Horn Point Laboratory, University of Maryland Center for Environmental Science, Cambridge, MD 21613, USA.
⁴ Marine Biological Section, University of Copenhagen, 3000 Helsingør, Denmark.
⁵ Institut de Ciències del Mar, CSIC. Pg Marítim de la Barceloneta 37-49, 08003, Barcelona, Spain.
⁶ Department of Marine Sciences, University of Connecticut, Groton CT, 06340, USA.
⁷ Department of Biology, Temple University, Philadelphia, PA 19122, USA.
⁸ Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089-0371, USA.
⁹ UPMC Université Paris 06, CNRS, Laboratoire Adaptation et Diversité en Milieu Marin UMR7144, Sorbonne Universités, Station Biologique de Roscoff, 29688 Roscoff, France.
¹⁰ Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 129, Hobart, Tasmania 7001, Australia.
¹¹ Hellenic Centre for Marine Research, Institute of Oceanography, 71003 Heraklion, Crete, Greece.
¹² Division of Plant Science, University of Dundee at the James Hutton Institute, Invergowrie, Dundee DD2 5DQ, UK.
¹³ Climate Change Cluster, University of Technology Sydney, Ultimo, New South Wales 2007, Australia.
¹⁴ Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
¹⁵ Department of Biology, University of Bergen, 5020 Bergen, Norway.

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.

MeSH terms

Chloroplasts / physiology
Eukaryota
Food Chain*
Oceans and Seas
Phototrophic Processes*
Plankton / physiology*
Spatio-Temporal Analysis
Symbiosis