MIXOTROPHIC NUTRITION OF PHYTOPLANKTON

Venus Fly Traps of the Microbial World

Phytoplankton are protists that photosynthesize using sunlight and CO₂ to obtain energy and produce organic matter. But there are phytoplankton that ingest other microorganisms in addition to photosynthesizing. These organisms can capture and digest prey including bacteria, cyanobacteria and other algae. Because they have the ability to obtain energy and materials at two trophic levels (i.e., they “mix” plant and animal nutrition in the same organism), they are often called “mixotrophic” as opposed to phototrophic (plant) or heterotrophic (animal). While the existence of mixotrophs has been known for over 100 years, relatively little was understood about their abundance or ecological impact until much more recently.  This lack of information is being remedied as many scientists throughout the world have begun to reconsider this  phenomenon during the last 20 years.

NSF funding to myself and co-PI Rebecca Gast of Woods Hole Oceanographic Institution has allowed us to investigate mixotrophy in plankton from the Antarctic and Arctic environments.  Recently we documented wide-spread occurrence of mixotrophy in the Ross Sea, Antarctica and also in the Arctic (see below). We will continue studying an Antarctic dinoflagellate that ingests phytoplankton and retains functional chloroplasts (kleptoplasty), a somewhat different alternative nutritional strategy. We also investigated the ecological impact of mixotrophs in a changing Arctic climate. Our current funding from the National Science Foundation is to study mixotrophs along the Western Antarctic Peninsula – south of Chile – as opposed to south of New Zealand in the Ross Sea.

In collaboration with co-workers, I previously explored the distribution, relative abundance, and feeding abilities of planktonic mixotrophs in lakes and the ocean. We also examined physiological attributes of isolated species in laboratory experiments.  Mixotrophy may afford algae with some advantages (relative to purely phototrophic or purely heterotrophic protists of similar size) in particular environmental situations. Specifically, mixotrophs’ ability to exploit two different forms of nutrition (phototrophy and heterotrophy) may allow them to cope with energy or nutrient limitation in nature. For example, most algae rely on the uptake of dissolved nutrients such as ammonia and phosphate to obtain sufficient nitrogen and phosphorus for growth. Mixotrophic algae may be able to obtain these elements by consuming prey and using the nitrogen and phosphorus from the digested prey (see selected references below). Other specific nutritional needs (vitamins, lipids) may also be gained via ingested prey.

As a part of our projects, we surveyed a number of freshwater and marine plankton communities to determine the abundances of mixotrophic algae in nature. We have looked in such disparate environments as George’s Bank off the New England coast, the Sargasso Sea near Bermuda, the Ross Sea and the Western Antarctic Peninsula (Antarctica), the Beaufort Sea (Arctic), the East China Sea, and in several lakes in Georgia and in the Pocono mountains of Pennsylvania. Mixotrophs are present in all of these environments, but their abundances vary tremendously over time and distance.

Protists– The term protist is used to group single-celled (mostly) eukaryotes from most of the groups formerly classified as algae, protozoa, and slime molds. It is a grouping of convenience since members of the group have polyphyletic origins. This means that they were derived from two or more ancestral groups.

REFERENCES. For more of our papers on mixotrophy, including links to abstracts and or PDF files, see “Publications.”

• Hamsher, S.E., K. Ellis, D. Holen and R.W. Sanders. 2020. Effects of light, dissolved nutrients and prey on ingestion and growth of a newly identified mixotrophic alga, Chrysolepidomonas dendrolepidota (Chrysophyceae). Hydrobiologia 847:2923-2932. [doi:10.1007/s10750-020-04293-z]
• Leles, S.G., A. Mitra, K.J. Flynn, U. Tillmann, D. Stoecker, H.J. Jeong, J. Burkholder, P.J. Hansen, D.A. Caron, P.M. Glibert, G. Hallegraeff, J. Raven, R.W. Sanders, M. Zubkov. 2019. Sampling bias misrepresents the biogeographic significance of constitutive mixotrophs across global oceans. Global Ecology and Biogeography 28:418-428. [doi: 10.1111/geb.12853]
• McKie-Krisberg, Z.M., R.W. Sanders and R.J. Gast. 2018. Evaluation of mixotrophy-associated gene expression in two species of polar marine algae. Frontiers in Marine Science 5:273.[doi: 10.3389/fmars.2018.00273]
• Gast, R.J., S.A. Fay and R.W. Sanders. 2018. Mixotrophic activity and diversity of Antarctic marine protists in austral summer. Frontiers in Marine Science 5:13.[doi: 10.3389/fmars.2018.00013]
• Princiotta, S.D. and R.W. Sanders. 2017. Heterotrophic and mixotrophic nanoflagellates in a mesotrophic lake: abundance and grazing impacts across season and depth. Limnology & Oceanography 62: 632-644.
• Princiotta, S.D., B. Smith and R.W. Sanders. 2016. Temperature-dependent phagotrophy and phototrophy in a mixotrophic chrysophyte. Journal of Phycology 52: 432-440.
• McKie-Krisberg, Z.M., R.J. Gast and R.W. Sanders. 2015. Physiological responses of three species of Antarctic mixotrophic phytoflagellates to changes in light and dissolved nutrients. Microbial Ecology 70:21-29.
• McKie-Krisberg, Z.M. and R.W. Sanders. 2014. Phagotrophy by the picoeukaryotic green alga Micromonas: implications for Arctic Oceans. ISME Journal 8:1953-1961.
• Sanders, R.W. and R.J. Gast. 2012. Bacterivory by phototrophic picoplankton and nanoplankton in Arctic waters. FEMS Microbiology Ecology 82:242-253.
• Tsai, A.Y., G.C. Gong, R.W. Sanders, W.H. Chen, C.F. Chao, and K.P. Chiang. 2011. Importance of bacterivory by pigmented and heterotrophic nanoflagellates during the warm season in a subtropical western Pacific coastal ecosystem. Aquatic Microbial Ecology 63:9-18.
• Moorthi S.D., D.A. Caron, R. Gast, and R.W. Sanders. 2009. Mixotrophy: a widespread and important ecological strategy for planktonic and sea-ice nanoflagellates in the Ross Sea, Antarctica. Aquatic Microbial Ecology 54:269-277.
• Gast, R.J., D.M. Moran, M.R. Dennett, and D.A. Caron. 2007. Kleptoplasty in an Antarctic dinoflagellate: caught in evolutionary transition? Environmental Microbiology 9:39-45.
• Sanders, R.W. 1991. Mixotrophic protists in marine and freshwater ecosystems. Journal of Protozoology 38: 76-81.
• Sanders, R.W. and K.G. Porter. 1988. Phagotrophic phytoflagellates. In: K.C. Marshall, (Ed.) Advances in Microbial Ecology 10: 167-192.
• Caron, D.A., R.W. Sanders, E.L. Lim, C. Marrasé, L.A. Amaral, S. Whitney, R. Aoki, and K.G. Porter. 1993. Light-dependent phagotrophy in the freshwater mixotrophic chrysophyte Dinobryon cylindricum. Microbial Ecology 25: 93-111.
• Sanders, R.W., U.G. Berninger, E.L. Lim, P.F. Kemp and D.A. Caron. 2000. Heterotrophic and mixotrophic nanoplankton predation on picoplankton in the Sargasso Sea and on Georges Bank. Marine Ecology Progress Series 192:103-118.
• Sanders, R.W., D.A. Caron, J.M. Davidson, M.R. Dennett, and D. Moran. 2001. Nutrient acquisition and population growth of a mixotrophic alga in axenic and bacterized cultures.  Microbial Ecology 42:513-523.