Comparative Quantitative Proteomics Reveals the Desiccation Stress Responses of the Intertidal Seaweed NEOPORPHYRA haitanensis

Abstract

Neoporphyra haitanensis is an economically important red seaweed that inhabits upper intertidal zones. The thallus tolerates extreme fluctuating environmental stresses (e.g., surviving more than 80% water loss during low tides). To elucidate the global molecular responses relevant to this outstanding desiccation tolerance, a quantitative proteomics analysis of N. haitanensis under different desiccation treatments as well as rehydration was performed. According to the clustering of expression patterns and the functional interpretation of the 483 significantly differentially expressed proteins, a three‐stage cellular response to desiccation stress and subsequent rehydration was proposed. Stage I: at the beginning of water loss, multiple signal transduction pathways were triggered including lipid signaling, protein phosphorylation cascades, and histone acetylation controlling acetate biosynthesis to further modulate downstream hormone signaling. Protein protection by peptidyl‐prolyl isomerase and ROS scavenging systems were also immediately switched on. Stage II: with the aggravation of stress, increases in antioxidant systems, the accumulation of LEA proteins, and the temporary biosynthesis of branched starch were observed. Multiple enzymes involved in redox homeostasis, including peroxiredoxin, thioredoxin, ascorbate peroxidase, superoxide dismutase, glutathione peroxidase, and glutathione reductase, were hypothesized to function in specific cellular compartments. Stage III: when the desiccated thalli had rehydrated for 30 mins, photosynthesis and carbon fixation were recovered, and antioxidant activities and protein structure protection were maintained at a high level. This work increases the understanding of the molecular responses to environmental stresses via a proteomic approach in red seaweeds and paves the way for further functional studies and genetic engineering.

Insights into agar and secondary metabolite pathways from the genome of the red alga Gracilaria domingensis (Rhodophyta, Gracilariales)

“…Our results relative to putative HGT events in Gracilaria domingensis are similar to that reported for the multicellular read alga Neopyropia yezoensis (Wang et al. 2020). In N. yezoensis 51 HGT‐derived genes were reported, with functions related to carbohydrate metabolism, transport, stress response, and antibiotic resistance.…”

Molecular response of Sargassum vulgare to acidification at volcanic CO2 vents: Insights from proteomic and metabolite analyses

“…Many studies have highlighted the impact of stress and environmental changes on the translation in some marine species (Anderson et al, 2015; Bailey et al, 2017; Chapman et al, 2011; Meistertzheim et al, 2007; Timmins‐Schiffman et al, 2014; Todgham & Hofmann, 2009; Tomanek et al, 2011; Wong et al, 2011). In particular, previous proteomic studies have reported the involvement of the translation process in stress response, like desiccation and subsequent rehydration in red macroalgae (Wang et al, 2020; Xu et al, 2016), high temperature in a green macroalga (Fan et al, 2018), as well as feedback to the nitrogen deprivation in a microalga (Garnier et al, 2014). Furthermore, transcripts related to information storage and processing were identified in some phytoplanktonic species under elevated pCO 2 (Benner et al, 2013; Beszteri et al, 2018; Hennon et al, 2015).…”

The red seaweed Asparagopsis taxiformis genome and integrative -omics analysis

“…For example, a transcriptomic-derived protein database in the red seaweed Eucheuma denticulatum enabled the proteomic characterisation of extracellular proteins following soluble protein extraction [19]. In the red seaweed Neoporphyra haitanensis, a genome-derived protein database was used to assess the proteins associated with molecular responses to environmental stresses [20].…”