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Abstract Mixotrophic protists combine photosynthesis and phagotrophy to obtain energy and nutrients. Because mixotrophs can act as either primary producers or consumers, they have a complex role in marine food webs and biogeochemical cycles. Many mixotrophs are also phenotypically plastic and can adjust their metabolic investments in response to resource availability. Thus, a single species's ecological role may vary with environmental conditions. Here, we quantified how light and food availability impacted the growth rates, energy acquisition rates, and metabolic investment strategies of eight strains of the mixotrophic chrysophyte,Ochromonas. All eightOchromonasstrains photoacclimated by decreasing chlorophyll content as light intensity increased. Some strains were obligate phototrophs that required light for growth, while other strains showed stronger metabolic responses to prey availability. When prey availability was high, all eight strains exhibited accelerated growth rates and decreased their investments in both photosynthesis and phagotrophy. Photosynthesis and phagotrophy generally produced additive benefits: In low‐prey environments,Ochromonasgrowth rates increased to maximum, light‐saturated rates with increasing light but increased further with the addition of abundant bacterial prey. The additive benefits observed between photosynthesis and phagotrophy inOchromonassuggest that the two metabolic modes provide nonsubstitutable resources, which may explain why a tradeoff between phagotrophic and phototrophic investments emerged in some but not all strains.
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Metabolic rewiring and biomass redistribution enable optimized mixotrophic growth in Chlamydomonas
Aquatic photosynthetic systems account for approximately one-half of all global carbon assimilation and could be a significant source of renewable fuels and feedstocks. However, rapid growth and biomass production in algae have not always translated into high product yields, partly because central metabolism is context specific, with metabolic fluxes being influenced by nutrient conditions and other environmental factors. In the green microalgaChlamydomonas reinhardtii(Chlamydomonas), mixotrophic cultures (acetate + light) grow far faster than phototrophic (light only) or heterotrophic (acetate + dark) cultures, even though acetate partially suppresses photosynthesis. Here, an isotopic dilution strategy with unlabeled acetate was combined with13CO2transient labeling to perform isotopically nonstationary metabolic flux analysis (INST-MFA) and to directly compare autotrophic and mixotrophic metabolism in Chlamydomonas supported by data from transcriptomics, proteomics, and metabolomics. INST-MFA indicated that acetate induces a synergistic rewiring of metabolism, conserving carbon by using the glyoxylate cycle and suppressing gluconeogenesis, the latter of which was discordant with omics results and prior models. Additionally, our data provide a plausible rationale for the well-known suppression of photosynthesis by acetate. We propose that reduced total protein content in mixotrophic versus phototrophic cells, much of which is attributed to reduced levels of photosynthetic proteins, decreases the costly metabolic burden of protein synthesis and represents a growth rate optimization strategy.
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- PAR ID:
- 10662719
- Publisher / Repository:
- PNAS
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 123
- Issue:
- 4
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1073/pnas.2522572123
