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Transcriptomic response of Daphnia magna to nitrogen- or phosphorus-limited diet.

ABSTRACT: Effects of nutrient-imbalanced diet on the growth and fitness of zooplankton were widely reported as key issues to aquatic ecology. However, little is known about the molecular mechanisms driving the physiological changes of zooplankton under nutrient stress.In this study, we investigated the physiological fitness and transcriptomic response of Daphnia magna when exposed to nitrogen (N)-limited or phosphorus (P)-limited algal diet (Chlamydomonas reinhardtii) compared to regular algae (N and P saturated).D. magna showed higher ingestion rates and overexpression of genes encoding digestive enzymes when fed with either N-limited or P-limited algae, reflecting the compensatory feeding. Under P-limitation, both growth rate and reproduction rate of D. magna were greatly reduced, which could be attributed to the downregulated genes within the pathways of cell cycle and DNA replication. Growth rate of D. magna under N-limitation was similar to normal group, which could be explained by the high methylation level (by degradation of methionine) supporting the body development.Phenotypic changes of D. magna under nutrient stress were explained by gene and pathway regulations from transcriptome data. Generally, D. magna invested more on growth under N-limitation but kept maintenance (e.g., cell structure and defense to external stress) in priority under P-limitation. Post-translational modifications (e.g., methylation and protein folding) were important for D. magna to deal with nutrient constrains.This study reveals the fundamental mechanisms of zooplankton in dealing with elemental imbalanced diet and sheds light on the transfer of energy and nutrient in aquatic ecosystems.

SUBMITTER: Xu Z

PROVIDER: S-EPMC8366849 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Increased population density may lead to a decrease in energy available for growth and reproduction via effects on the activity level of individuals. Whilst this may be of particular importance for organisms that compete for defendable resources and/or have a high frequency of social interactions, it is less obvious how individual activity should covary with population density when food resources are not defendable or direct interactions among individuals are negligible. Based on observations that there is a general negative relationship between population density and metabolism it has been suggested that organisms actively reduce activity under increased density to accommodate an expected decrease in food availability. However, in the absence of direct activity measurements the validity of this hypothesis is unclear. Here we test for such anticipatory adjustments of activity levels in the planktonic cladoceran Daphnia magna Straus, a filter feeder whose food resources are not defendable, meaning that density responses can be evaluated in the absence of direct interactions. We tested for changes in activity in response to two separate density cues, one being the direct physical and visual stimuli resulting from being in the vicinity of conspecifics ('direct density experiment'), and the other being the detection of olfactory cues in their environment ('olfactory cue experiment'). Ten genetically distinct clones were used to evaluate the potential for genetic variation in these responses. Our measures of activity were highly repeatable, and there was significant variation in activity among clones. Furthermore, this clonal variation was consistent in the 'direct density' and 'olfactory cue' experiments. The estimated evolvability of the trait (1.3-3.2%) was within the range typically observed in behavioural traits. However, there was no indication that the activity level of individuals respond to population density, either directly to actual density or to olfactory cues representing high density. In this case, the energetic influence of density on population dynamics is sufficiently described by effects on per capita resource availability.

Project description:BACKGROUND:The role of coastal nutrient sources in the persistence of Karenia brevis red tides in coastal waters of Florida is a contentious issue that warrants investigation into the regulation of nutrient responses in this dinoflagellate. In other phytoplankton studied, nutrient status is reflected by the expression levels of N- and P-responsive gene transcripts. In dinoflagellates, however, many processes are regulated post-transcriptionally. All nuclear encoded gene transcripts studied to date possess a 5' trans-spliced leader (SL) sequence suggestive, based on the trypanosome model, of post-transcriptional regulation. The current study therefore sought to determine if the transcriptome of K. brevis is responsive to nitrogen and phosphorus and is informative of nutrient status. RESULTS:Microarray analysis of N-depleted K. brevis cultures revealed an increase in the expression of transcripts involved in N-assimilation (nitrate and ammonium transporters, glutamine synthetases) relative to nutrient replete cells. In contrast, a transcriptional signal of P-starvation was not apparent despite evidence of P-starvation based on their rapid growth response to P-addition. To study transcriptome responses to nutrient addition, the limiting nutrient was added to depleted cells and changes in global gene expression were assessed over the first 48 hours following nutrient addition. Both N- and P-addition resulted in significant changes in approximately 4% of genes on the microarray, using a significance cutoff of 1.7-fold and p ? 10-4. By far, the earliest responding genes were dominated in both nutrient treatments by pentatricopeptide repeat (PPR) proteins, which increased in expression up to 3-fold by 1 h following nutrient addition. PPR proteins are nuclear encoded proteins involved in chloroplast and mitochondria RNA processing. Correspondingly, other functions enriched in response to both nutrients were photosystem and ribosomal genes. CONCLUSIONS:Microarray analysis provided transcriptomic evidence for N- but not P-limitation in K. brevis. Transcriptomic responses to the addition of either N or P suggest a concerted program leading to the reactivation of chloroplast functions. Even the earliest responding PPR protein transcripts possess a 5' SL sequence that suggests post-transcriptional control. Given the current state of knowledge of dinoflagellate gene regulation, it is currently unclear how these rapid changes in such transcript levels are achieved.

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Transcriptomic response of Daphnia magna to nitrogen- or phosphorus-limited diet.

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