Sweet and fatty symbionts: photosynthetic productivity and carbon storage boosted in microalgae within a host
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Abstract
Symbiosis between a host and intracellular eukaryotic microalgae is a widespread life strategy in aquatic ecosystems. This partnership is considered to be mainly energized by the photosynthetically-derived carbon energy of microalgal symbionts. A major question is whether microalgae increase their photosynthetic production and decrease carbon storage in order to maximize carbon translocation to their host. By combining three-dimensional subcellular imaging and physiological analyses, we show that the photosynthetic machinery (chloroplast and CO 2 -fixing pyrenoid) of the symbiotic microalga Micractinium conductrix significantly expands inside their host (the ciliate Paramecium bursaria ) compared to the free-living state. This is accompanied by a 13-fold higher quantity of Rubisco enzymes and 16-fold higher carbon fixation rate. Time-resolved subcellular imaging revealed that photosynthetically-derived carbon is first allocated to starch during the day, with five times higher production in symbiosis despite low growth. Nearly half of the carbon stored in starch is consumed overnight and some accumulates in lipid droplets, which are 20-fold more voluminous in symbiotic microalgae. We also show that carbon is transferred to the host and hypothesize that much of this is respired by the high density of surrounding host mitochondria. We provide evidence that the boosted photosynthetic production of symbiotic microalgae could be explained by the energetic demands of the host. Overall, this study provides an unprecedented view of the subcellular remodeling and dynamics of carbon metabolism of microalgae inside a host, highlighting the potentially key role of the source-sink relationship in aquatic photosymbiosis.
Significance statement
Symbiotic interactions between a heterotrophic host and intracellular microalgae are widespread in aquatic ecosystems and are considered to be energized by the photosynthetically-derived carbon energy. However, little is known on the impact of symbiosis on the algal bioenergetics (e.g. carbon production and storage). This study reveals the morphological and physiological changes of a microalga inside a host at the subcellular scale over the day. We show that the photosynthetic machinery expands and carbon fixation and storage are boosted in symbiotic microalgae beyond their growth needs. This high photosynthetic production is very likely enhanced by the host energetic demands. Our findings advance our basic understanding of photosymbiosis and open new perspectives on the mechanisms and drivers of metabolic exchange between partners.
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Conclusion and Perspectives
Thank you for sharing this impressive piece of work! It is amazing how the entire function and morphology of a cell can change based on its environment! The use of multiple high-resolution techniques all converging on a consistent conclusion is very convincing!
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Cell volume was 5.6-fold higher than the free-living stage (43.55 ± 12.97 µm3 vs 7.79 ± 1.94 µm3).
This is very striking and interesting! We noticed a similar phenotype in the species Chlamydomonas smithii when we grew them in nutrient rich marine broth (https://doi.org/10.57844/arcadia-35f0-3e16). The cells became much larger compared to when grown in standard low-nutrient TAP media. Do you think this could have anything to do with increased nutrient availability within the host cell?
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liquid medium
Is this the same bacterized volvic natural mineral water supplemented w/ protozoan pellets that the P. bursaria are grown in? or liquid HSM? or different media? just wondering if there are any external nutrients contributing to any of the differences.
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Released symbiotic microalgae were recovered after filtration through a 40 µm cell strainer and 10 µm filter that removed host debris. The filtrate was centrifuged (2 min at 2 500 g) and plated on modified solid High Salt Medium (HSM) (Gorman and Levine 1965; Sueoka 1960). Microalgae were maintained at 20°C with a 12:12 h light/dark cycle - light intensity of 40 μE m−2 s−1 - and re-streaked on plates every week.
Interesting! Since the average volume of the symbiotic algae was ~43 um, do you think you're selecting for smaller cells from the start?
For the symbiotic algae in the study, were the isolated M. conductrix cultures re-introduced into vacant P. bursaria cells to correct for any inadvertent size selection?
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The most important differences involved the energy-producing organelles, with the volume of the chloroplast and mitochondrion increasing 6.4 and 7.3-fold in symbiotic microalgae, respectivel
In your FIB-SEM, did you notice any differences in the cell wall of the free-living vs symbiotic algae? Has the 5.6-fold larger cell lost the wall, which might not be as necessary anymore since it has a protective host?
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