Metabolic regulatory oscillations in intertidal green seaweed Ulva lactuca against tidal cycles

Vishal Gupta,Hemant R Kushwaha

doi:10.1038/s41598-017-15994-2

Vishal Gupta, Hemant R Kushwaha

Open Access

https://doi.org/10.1038/s41598-017-15994-2

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Abstract

The survival of wetland plant species largely relies on physiological adaptations essential for submergence and desiccation. Intertidal seaweeds, unlike terrestrial plants, have unique adaptations to submergence and can also sustain desiccation arising from tidal rhythms. This study determined the differential metabolic regulations in the inter-tidal seaweed species Ulva lactuca against the submergence and desiccation. During desiccation, the relative water content of the algal thalli declined with concomitant increase in reactive oxygen species (ROS) and lipid peroxidation. Nevertheless, the trends reversed during recovery on re-submergence and attained homeostasis. Metabolite profiling of U. lactuca revealed desiccation induced balance in energy reserve utilization by adjusting carbohydrate metabolism and switch over to ammonia metabolism. Upon re-submergence, thalli showed an increase in fermentative metabolites, pyruvate-alanine conversion, and the GABA shunt. Prolonged submergence induced substrate level phosphorylation mediated sugar biosynthesis while continuing the alternative carbon flux through fermentative metabolism, an increase in osmoprotectants glycine and betaine, sulfur bearing compounds cysteine and hypotaurine, and phenolic compound coniferaldehyde. The determined metabolic regulations in U. lactuca for submergence tolerance provide insights into potential evolutionarily conserved protective mechanisms across the green lineage and also highlights the possible role of sulfur oxoforms as strong free radical scavengers.

Highlights

Marine macroalgae represent the earliest diverging and evolutionary diverse aquatic organism occupying the basal position in the aquatic food web of intertidal and subtidal regions[1]
On re-submergence after the desiccation time points of 12, 24, 36, 48 and 72 h, algae could able to recover and grow normally. This indicates that the relative water content (RWC) decline to less than 50% allow U. lactuca to recover on submergence
This study for the first time revealed the differential metabolic regulations in intertidal seaweed species U. lactuca against desiccation-submergence cycle arising from periodic tidal rhythms

Summary

Introduction

Marine macroalgae (seaweeds) represent the earliest diverging and evolutionary diverse aquatic organism occupying the basal position in the aquatic food web of intertidal and subtidal regions[1] This group of aquatic plants have the unique physiology of being able to grow in fully submerged conditions representing the contrasting homeostasis regulations over land plants. The natural adaptation of Ulva species to submergence and desiccation represents the existence of a unique homeostasis regulation. Unlike terrestrial crops, Ulva has simple diastromatic thallus without any complex cellular level organization This implies that the adaptive regulations are mostly cellular responses as opposed to complex anatomic modification in other plants to tolerate submergence. The present study is an attempt to understand the unique adaptation of Ulva lactuca tolerating periodic desiccation-submergence cycle using a holistic approach of untargeted metabolomics. A ‘learn from nature approach’ using a model organism naturally adapted for submergence and exposure, such as seaweed, can be supportive in understanding the submergence tolerance mechanisms either evolutionarily conserved or unique

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