Metabolic plasticity of mixotrophic algae is key for their persistence in browning environments

Abstract

Light availability is the main regulator of primary production, shaping photosynthetic communities and their production of ecologically important biomolecules. In freshwater ecosystems, increasing dissolved organic carbon (DOC) concentrations, commonly known as browning, leads to lower light availability and the proliferation of mixotrophic phytoplankton. Here, a mixotrophic algal species (Cryptomonas sp.) was grown under five increasing DOC concentrations to uncover the plastic responses behind the success of mixotrophs in browning environments and their effect in the availability of nutritionally important biomolecules. In addition to the browning treatments, phototrophic, heterotrophic and mixotrophic growth conditions were used as controls. Despite reduced light availability, browning did not impair algal growth compared to phototrophic conditions. Comparative transcriptomics showed that genes related to photosynthesis were down‐regulated, whereas phagotrophy gene categories (phagosome, lysosome and endocytosis) were up‐regulated along the browning gradient. Stable isotope analysis of phospholipid fractions validated these results, highlighting that the studied mixotroph increases its reliance on heterotrophic processes with browning. Metabolic pathway reconstruction using transcriptomic data suggests that organic carbon is acquired through phagotrophy and used to provide energy in conjunction with photosynthesis. Although metabolic responses to browning were observed, essential fatty acid content was similar between treatments while sterol content was slightly higher upon browning. Together, our results provide a mechanistic model of how a mixotrophic alga responds to browning and how such responses affect the availability of nutritionally essential biomolecules for higher trophic levels.

Lake browning counteracts cyanobacteria responses to nutrients: Evidence from phytoplankton dynamics in large enclosure experiments and comprehensive observational data

“…This may explain why the dominant cyanobacterium Phillips et al, 2013). This suggests mixotrophy as the most plausible species trait accounting for the success of cryptophytes in the brown enclosures (Calderini et al, 2022;Grujcic et al, 2018;Hansson et al, 2019). Increasing dominance of mixotrophic phytoplankton under conditions of browning in stratified lakes has also been repeatedly reported by others (Bergström et al, 2003;Deininger et al, 2017;Wilken et al, 2018).…”

The second life of terrestrial and plastic carbon as nutritionally valuable food for aquatic consumers

“…Limitations of inorganic carbon and light may be overcome by utilizing terrestrial organic carbon (Calderini et al, 2022;Tittel et al, 2009). In addition to highly labile terrestrial carbohydrates, freshwater ecosystems also receive potentially recalcitrant organic carbon sources, for example lignocellulose, which forms 80 to 90% of terrestrial inputs to lakes and rivers (Brett et al, 2017;Jones, 1992).…”

“…However, in these experiments, light has been available, and thus, it is uncertain whether the actual biosynthesis of essential biomolecules occurs only under light (autotrophy). Based on the previous literature (Glibert & Legrand, 2006), it seems that almost all phytoplankton species are capable of osmotrophy and thus could utilize terrestrial dissolved organic carbon (DOC) (Tittel et al, 2009) or plastic leachates (Sheridan et al, 2022), and thus could integrate autochthonous, allochthonous and anthropogenic carbon sources in aquatic food webs (Calderini et al, 2022;Granéli et al, 1999;Selosse et al, 2017;Tittel et al, 2009).…”

Organic compounds drive growth in phytoplankton taxa from different functional groups

“…Combining autotrophic and heterotrophic mechanisms might enable phytoplankton to maintain growth, especially under highly variable and partially stressful conditions such as light limitation, which is common in estuaries and similar habitats (20). Different studies have found mixotrophy to be associated with reduced light availability, which has largely been investigated for phagotrophs (9,23) and benthic diatoms (24). Some phytoplankton taxa have been shown to even survive complete darkness on the basis of organic carbon (4,25).…”

“…The utilisation of organic compounds in such ecosystems might be critical for phytoplankton to maintain growth, especially where light is limited as a consequence of high loads of suspended matter. Different phytoplankton taxa have been shown to survive and grow based on organic carbon in the dark and at reduced light levels (4,9,23–25). Hence, unsurprisingly, the importance of mixotrophic taxa in estuarine ecosystems has been reported in several studies (26–29).…”