Organic compounds drive growth in phytoplankton taxa from different functional groups

Abstract

Phytoplankton are usually considered autotrophs, but an increasing number of studies show that many taxa are able also to use organic carbon. Acquiring nutrients and energy from different sources might enable an efficient uptake of required substances and provide a strategy to deal with varying resource availability, especially in highly dynamic ecosystems such as estuaries. In our study, we investigated the effects of 31 organic carbon sources on the growth (proxied by differences in cell counts after 24 h exposure) of 17 phytoplankton strains from the Elbe estuary spanning four functional groups. All of our strains were able to make use of at least 1 and up to 26 organic compounds for growth. Pico-sized green algae such as Mychonastes, as well as the nano-sized green alga Monoraphidium in particular were positively affected by a high variety of substances. Reduced light availability, typically appearing in turbid estuaries and similar habitats, resulted in an overall poorer ability to use organic substances for growth, indicating that organic carbon acquisition was not primarily a strategy to deal with darkness. Our results give further evidence for mixotrophy being a ubiquitous ability of phytoplankton and highlight the importance to consider this trophic strategy in research.

Keywords: estuary; green algae; mixotrophy; picophytoplankton.

Figure 2.

Number of significantly negative (a) and positive (b) effects (t-test, p ≤ 0.05; electronic supplementary material, table S3) of organic compounds on the growth of phytoplankton and effect ratio (strength) (c) across three plate replicates per strain and light treatment. The x-axis shows the taxa, including various strains in some cases, and light treatment (indicated by colour). For example, we included three different strains of Mychonastes, while one of them—P4—was included with different light treatments. Strain names N7 and P4 are shown explicitly as needed for further description. In (a), numbers for fewer than five significant effects are omitted for clarity. (c) Includes all effects independent of their significance per strain and light treatment, i.e. every single measurement normalized by the control of the respective plate. This is presented by relative values around 0. Each boxplot consists of 279 values (31 substances × 3 well replicates × 3 plate replicates). Where relevant, we highlight where the ratios of the different light treatment groups were significantly different (t-test, *p ≤ 0.05) in (c). n.s., not significant.

Figure 1.

Experimental set-up (a) and data processing and analysis (b). ‘Light' and ‘dark' refer to the condition of the light phase of the 12 h : 12 h light : dark cycle, which were ca 150 µmol photons s⁻¹ m⁻²) in the light treatment and ca 75% reduced in the dark treatment. Amp = ampicillin (100 µg ml⁻¹) added ca 5 days prior to measurements. The horizontal axes in (b) show the control and different organic compounds, as can be obtained from the supplementary information (electronic supplementary material, figures S1.1–S1.24). Significance refers to the comparison of an organic treatment with the control without added organic compounds.

Figure 3.

Number of significantly negative (a) and positive (b) effects (t-test, p ≤ 0.05; electronic supplementary material, table S3) of different types of organic compounds on the growth of the 17 phytoplankton strains in the light (three plates per strain) and effect ratio (strength) (c). The ‘+' and ‘−’ indicate how the number of significant effects changed from light to dark (two weeks incubation), referring to the four strains included in the dark experiment, namely Mychonastes (strain P4), Tetradesmus, Choricystis and Monoraphidium (strain N7). Precisely, ‘+' indicates an increase of significant effects from light to dark and ‘−' indicates a decrease of significant effects from light to dark. Note the varying numbers of compounds included per substrate type described in the methods. (c) Includes all effects, independent of their significance per strain and light treatment, i.e. every single measurement normalized by the control of the respective plate. This is presented by relative values around 0. The number of data points included in the box plots varied from ca 300 to ca 1500 depending on the number of substrates included per substrate type.