Integrative biological analyses of responses to food deprivation reveal resilience mechanisms in sea urchin larvae.

Abstract

A fundamental question in ecology is how organisms survive food deprivation. In the ocean, climate change is impacting the phenology of food availability for early life-history stages of animals. In this study, we undertook an integrative analysis of larvae of the sea urchin Strongylocentrotus purpuratus-an important keystone species in marine ecology and a molecular biological model organism in developmental biology. Specifically, to identify the mechanisms of resilience that maintain physiological state and the ability of organisms to recover from food deprivation, a suite of molecular biological, biochemical, physiological and whole organism measurements was completed. Previous studies focused on the importance of energy reserves to sustain larvae during periods of food deprivation. We show, however, that utilization of endogenous energy reserves only supplied 15% of the metabolic requirements of long-term survival (up to 22 days) in the absence of particulate food. This large energy gap was not supplied by larvae feeding on bacteria. Estimates of larval ability to transport dissolved organic matter directly from seawater showed that such substrates could fully supply metabolic needs. Integrative approaches allowed for filtering of gene expression signatures, linked with gene network analyses and measured biochemical and physiological traits, to identify biomarkers of resilience. We identified 14 biomarkers related to nutrition-responsive gene expression, of which a specific putative amino acid transporter gene was quantified in a single larva experiencing continuous nutritional stress. Advances in applications of gene expression technologies offer novel approaches to determine the physiological state of marine larval forms in ecological settings undergoing environmental change.