Metabolic flexibility during a trophic transition reveals the phenotypic plasticity of greater duckweed (Spirodela polyrhiza 7498)

Abstract

The greater duckweed (Spirodela polyrhiza 7498) exhibits trophic diversity (photoautotrophic, heterotrophic, photoheterotrophic, and mixotrophic growth) depending on the availability of exogenous organic carbon sources and light.Here, we show that the ability to transition between various trophic growth conditions is an advantageous trait, providing great phenotypic plasticity and metabolic flexibility in S. polyrhiza 7498.By comparing S. polyrhiza 7498 growth characteristics, metabolic acclimation, and cellular ultrastructure across these trophic modes, we show that mixotrophy decreases photosynthetic performance and relieves the CO 2 limitation of photosynthesis by enhancing the CO 2 supply through the active respiration pathway. Proteomic and metabolomic analyses corroborated that S. polyrhiza 7498 increases its intracellular CO 2 and decreases reactive oxygen species under mixotrophic and heterotrophic conditions, which substantially suppressed the wasteful photorespiration and oxidative-damage pathways. As a consequence, mixotrophy resulted in a higher biomass yield than the sum of photoautotrophy and heterotrophy.Our work provides a basis for using trophic transitions in S. polyrhiza 7498 for the enhanced accumulation of value-added products.

Survival Strategies of Duckweeds, the World’s Smallest Angiosperms

“…Although duckweeds generally grow photoautotrophically, using light and mineral salts for photosynthesis, they can also grow mixotrophically in light with sugars and even heterotrophically in the dark if sufficient sugars, amino acids, and vitamins are available in the medium [2,3,47,75]. The ability to transition between different trophic conditions was shown to endow S. polyrhiza with great metabolic flexibility [76]. Duckweed mixotrophy and heterotrophy are of commercial interest in the context of the production of starchrich biomass [72], and especially mixotrophy is thought to be much more widespread in nature than previously thought [77].…”

Glycogen synthesis prevents metabolic imbalance and disruption of photosynthetic electron transport from photosystem II during transition to photomixotrophy in Synechocystis sp. PCC 6803

“…2b,c) but eventually, over several days, reduces the photosynthetic capacity (Solymosi et al ., 2020). Similarly, starch accumulation and subsequent limitations in photosynthetic capacity were observed in the monocot Spirodela polyrhiza 7498 after glucose addition (Sun et al ., 2023). During this acclimation, glycogen becomes essential since impairments in the glycogen synthesis pathway, such as those in the ΔPGM and ΔAGP mutants, result in reduced fitness in the presence of glucose (Figs 2–4, 6, 7, S3, Gründel et al ., 2012).…”

Mechanisms of metabolic adaptation in the duckweed Lemna gibba: an integrated metabolic, transcriptomic and flux analysis

“…Under normal atmospheric conditions, about 25% of the reaction catalyzed by RuBisCO is oxygenation [ 96 ]. It has been reported for the duckweed Spirodela polyrhiza that under photomixotrophy, when organic carbon substrates are available and may be catabolized, RuBisCO oxygenation and operation of the photorespiratory pathway are most likely largely suppressed due to elevated intracellular CO 2 levels [ 3 ]. Therefore, in our model simulations, photorespiration was suppressed by setting the ratio of carboxylation flux to oxygenation flux to 1000:1.…”