Colonization of land from marine environments was a major transition for biological life on Earth, and intertidal adaptation was a key evolutionary event in the transition from marine- to land-based lifestyles. Multicellular intertidal red algae exhibit the earliest, systematic, and successful adaptation to intertidal environments, with Porphyra sensu lato (Bangiales, Rhodophyta) being a typical example. Here, a chromosome-level 49.67 Mbp genome for Neoporphyra haitanensis comprising 9,496 gene loci is described based on Meta-Hi-C-assisted whole genome assembly, which allowed the isolation of epiphytic bacterial genome sequences from a seaweed genome for the first time. The compact, function-rich N. haitanensis genome revealed that ancestral lineages of red algae share common horizontal gene transfer (HGT) events and close relationships with epiphytic bacterial populations. Specifically, the ancestor of N. haitanensis obtained unique lipoxygenase family genes from bacteria for complex chemical defense, carbonic anhydrases for survival in shell-borne conchocelis lifestyle stages, and numerous genes involved in stress tolerance. Combined proteomic, transcriptomic, and metabolomic analyses revealed complex regulation of rapid responses to intertidal dehydration/rehydration cycling within N. haitanensis. These adaptations include rapid regulation of its photosynthetic system, a readily available capacity to utilize ribosomal stores, increased methylation activity to rapidly synthesize proteins, and a strong anti-oxidation system to dissipate excess redox energy upon exposure to air. These novel insights into the unique adaptations of red algae to intertidal lifestyles inform our understanding of adaptations to intertidal ecosystems and the unique evolutionary steps required for intertidal colonization by biological life.

Background Red algae Porphyra sensu lato grow naturally in the unfavorable intertidal environment, in which they are exposed to substantial temperature fluctuations. The strategies of Porphyra to tolerate cold stress are poorly understood. Results Herein, investigations revealed that chilling and freezing induced alterations in the physiological properties, gene transcriptional profiles and metabolite levels in the economically important red algae species, Neoporphyra haitanensis. Control samples (kept at 20 °C) were compared to chilled thalli (10 and 4 °C) and to thalli under − 4 °C conditions. Chilling stress did not affect the health or photosynthetic efficiency of gametophytes, but freezing conditions resulted in the arrest of growth, death of some cells and a decrease in photosynthetic activity as calculated by Fv/Fm. Transcriptome sequencing analysis revealed that the photosynthetic system was down-regulated along with genes associated with carbon fixation and primary metabolic biosynthesis. Adaptive mechanisms included an increase in unsaturated fatty acids levels to improve membrane fluidity, an increase in floridoside and isofloridoside content to enhance osmotic resistance, and an elevation in levels of some resistance-associated phytohormones (abscisic acid, salicylic acid, and methyl jasmonic acid). These physiochemical alterations occurred together with the upregulation of ribosome biogenesis. Conclusions N. haitanensis adopts multiple protective mechanisms to maintain homeostasis of cellular physiology in tolerance to cold stress.

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Background Seaweeds in the upper intertidal zone experience extreme desiccation during low tide, followed by rapid rehydration during high tide. Porphyra sensu lato are typical upper intertidal seaweeds. Therefore, it is valuable to investigate the adaptive mechanisms of seaweed in response to dehydration-rehydration stress. Results A reduction in photosynthetic capacity and cell shrinkage were observed when N. haitanensis was dehydrated, and such changes were ameliorated once rehydrated. And the rate and extent of rehydration were affected by the air flow speed, water content before rehydration, and storage temperature and time. Rapid dehydration at high air-flow speed and storage at − 20 °C with water content of 10% caused less damage to N. haitanensis and better-protected cell activity. Moreover, proteomic and metabolomic analyses revealed the abundance members of the differentially expressed proteins (DEPs) and differentially abundant metabolites (DAMs) mainly involved in antioxidant system and osmotic regulation. The ascorbic acid-glutathione coupled with polyamine antioxidant system was enhanced in the dehydration response of N. haitanensis. The increased soluble sugar content, the accumulated polyols, but hardly changed (iso)floridoside and insignificant amount of sucrose during dehydration indicated that polyols as energetically cheaper organic osmolytes might help resist desiccation. Interestingly, the recovery of DAMs and DEPs upon rehydration was fast. Conclusions Our research results revealed that rapid dehydration and storage at − 20 °C were beneficial for recovery of N. haitanensis. And the strategy to resist dehydration was strongly directed toward antioxidant activation and osmotic regulation. This work provided valuable insights into physiological changes and adaptative mechanism in desiccation, which can be applied for seaweed farming.

Background Algae respond to chemical and environmental stimuli in a way similar to higher plants. However, their receptors sensing stimuli remain a mystery. Results We identified and characterized one putative abscisic acid-G-protein coupled receptor homologous protein from red alga Pyropia haitanensis, Ph1205, and analyzed its evolution relationship, subcellular localization, and ligand-binding properties. Ph1205 contains 9 predicted transmembrane domains. Phylogenetic analysis revealed its early evolution. Recombinant expression of Ph1205-Egfp in HEK293T cells and immunofluorescence detection against N-terminal extracellular 14 amino acids (N14) of Ph1205 in Ph1205-transfected HEK293T cells and P. haitanensis protoplast confirmed its membrane location. Both N14 and Ph1205-transfected cells displayed high affinity with salicylic acid (SA) and oligoagar, which activated cAMP response element in HEK293T cells and upregulated luciferase activity. SA and oligoagar elicited similar but different transcriptional profiles of P. haitanensis, mainly by being involved in anabolic metabolism and cell growth. However, related intracellular signaling system in P. haitanensis has not yet fully evolved and evidently responded. Conclusions Our results demonstrate that Ph1205 displays some structural and functional characteristics as an early evolutionary membrane receptor, has potential extracellular-binding affinity to SA and oligoagar, and can activate heterotrimeric G-protein and CRE in animal cells.