Deuterium in marine organic biomarkers: toward a new tool for quantifying aquatic mixotrophy

Abstract

The traditional separation between primary producers (autotrophs) and consumers (heterotrophs) at the base of the marine food web is being increasingly replaced by the paradigm that mixoplankton, planktonic protists with the nutritional ability to use both phago(hetero)trophy and photo(auto)trophy to access energy are widespread globally. Thus, many 'phytoplankton' eat, while 50% of 'protozooplankton' also perform photosynthesis. Mixotrophy may enhance primary production, biomass transfer to higher trophic levels and the efficiency of the biological pump to sequester atmospheric CO₂ into the deep ocean. Although this view is gaining traction, science lacks a tool to quantify the relative contributions of autotrophy and heterotrophy in planktonic protists. This hinders our understanding of their impacts on carbon cycling within marine pelagic ecosystems. It has been shown that the hydrogen (H) isotopic signature of lipids is uniquely sensitive to heterotrophy relative to autotrophy in plants and bacteria. Here, we explored whether it is also sensitive to the trophic status in protists. The new understanding of H isotope signature of lipid biomarkers suggests it offers great potential as a novel tool for quantifying the prevalence of mixotrophy in diverse marine microorganisms and thus for investigating the implications of the 'mixoplankton' paradigm.

Keywords: biomarker; carbon cycle; hydrogen; isotope; mixoplankton; mixotrophy; protist.

Fig. 1

Mixoplanktonic dinoflagellate Dinophysis caudata. The concept of animal and vegetable gets blurred when applied to unicellular organisms. Dinoflagellates can perform photosynthesis while devouring prey by phagocytosis and consuming dissolved organic molecules via osmotrophy. This latter mechanism is ubiquitous in phytoplankton. Photo by Nicolas Chomérat & Véronique Séchet (Ifremer).

Fig. 2

Schematic view of H flow during processes leading to lipids, polysaccharides and nonstructural carbohydrates (NSC) ²H‐ε_bio. The key enzymes and pathways responsible for H flow are indicated by their following abbreviations and are based on known biochemical pathways: 2‐OGDH, 2‐oxoglutarate dehydrogenase; 6PGD, 6‐phosphogluconate dehydrogenase; ACP, acyl carrier protein; ALD, aldolase; ENO, enolase; FNR, ferredoxin‐NADP⁺ reductase; G6PDH, glucose‐6‐phosphate dehydrogenase; GAPDH, glyceraldehyde 3‐phosphate dehydrogenase; KA, ketoacyl; ME, malic enzyme; NADP, nicotinamide adenine dinucleotide; NADPH, nicotinamide adenine dinucleotide phosphate; oxPPP, oxidative pentose phosphate pathway; PDH, pyruvate dehydrogenase; PGI, phosphoglucose isomerase; PK, pyruvate kinase; R, reductase; RuBisCO, ribulose‐1,5‐bisphosphate carboxylase/oxygenase; TE, trans‐enoyl; TPI, triosephosphate isomerase; and TPT, triose phosphate translocator. Simplified from Cormier et al. (2018) and references therein.

Fig. 3

Average δ²H values of fatty acids (methyl esterified) produced by Chlorella sorokiniana under different metabolic conditions. For the heterotrophic mode, C. sorokiniana was fed with glucose in the dark. C16 and C18 correspond to palmitic and stearic acid, respectively. Error bars correspond to ± SD (n = 3).

Fig. 4

Overview of the processes affecting δ²H values of lipid biomarkers in protists, where they take place (wiggly arrows), and their current level of understanding (inspired by Sachse et al., 2012). To effectively use δ²H values as a tool to quantify mixotrophic processes, key limitations in their understanding need to be resolved.