Single-Cell View of Carbon and Nitrogen Acquisition in the Mixotrophic Alga Prymnesium parvum (Haptophyta) Inferred From Stable Isotope Tracers and NanoSIMS

Nutritional modes of unicellular eukaryotes range from pure photoautotrophy of some phytoplankton to pure heterotrophy of species typically called protozoa. Between these two extremes lies a functional continuum of nutrient and energy acquisition modes termed mixotrophy. Prymnesium parvum is an ecol...

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Published inFrontiers in Marine Science Vol. 5
Main Authors Carpenter, Kevin J., Bose, Maitrayee, Polerecky, Lubos, Lie, Alle A. Y., Heidelberg, Karla B., Caron, David A.
Format Journal Article
LanguageEnglish
Published Lausanne Frontiers Research Foundation 11.05.2018
Frontiers Media S.A
Subjects
Algae
Biogeochemistry
Blooms
Carbon
Cells
Environmental changes
Fish
Food webs
Gene expression
haptophyte
Heterotrophy
Imaging techniques
Interspecific relationships
Mass mortality
Mass spectrometry
Mass spectroscopy
Mixotrophy
NanoSIMS
Nitrogen
Nitrogen isotopes
Nutrition
Photoautotrophy
Photosynthesis
Phytoplankton
Predation
protist
Protozoa
Prymnesium parvum
Ratios
Species diversity
Stable isotopes
Toxins
Tracers
United States > US
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Summary:Nutritional modes of unicellular eukaryotes range from pure photoautotrophy of some phytoplankton to pure heterotrophy of species typically called protozoa. Between these two extremes lies a functional continuum of nutrient and energy acquisition modes termed mixotrophy. Prymnesium parvum is an ecologically important mixotrophic haptophyte alga that can produce toxins and form ecosystem disruptive blooms that result in fish kills and changes in planktonic food web structure. We investigated carbon and nitrogen acquisition strategies of single cells of P. parvum using a combined experimental-imaging approach employing labeling of live cells with stable isotope tracers (13C and 15N) followed by measurement of cellular isotopic ratios using nanometer-scale secondary ion mass spectrometry (NanoSIMS). With this method, we were able to quantify the relative contributions of photosynthesis and heterotrophy to the nutrition of the alga. Our results suggest that P. parvum relies on predation primarily for nitrogen, while most carbon for cellular building blocks is obtained from inorganic sources. Our analysis further revealed that nitrogen assimilation can vary up to an order of magnitude among individual cells, a finding that would be difficult to determine using other methods. These results help to improve our understanding of mixotrophy across the enormous diversity of eukaryotes, one cell and one species at a time.
ISSN:2296-7745
2296-7745
DOI:10.3389/fmars.2018.00157