The life of crustaceans in water with low oxygen content suggests that there is more than one way to survive hypoxia



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CORVALLIS, Oregon – A puddle's ability to survive oxygen deprivation, while lacking a key set of genes, raises the possibility that animals may have more ways of dealing with hypoxic environments than previously thought.

Published in the Annals of the National Academy of Sciences, the findings of Oregon State University researchers are important because hypoxia – low oxygen areas – is increasing in waters around the globe, primarily because of human-caused factors such as agricultural runoff, fossil fuel burning and wastewater treatment effluent.

Hypoxia presents a major physiological challenge for animals, whose evolutionary history includes the development of cellular mechanisms to address changes in oxygen availability. The HIF pathway – hypoxia inducible factor – is the primary mechanism that animals use to detect and regulate oxygen levels.

Pacific Coast crustacean Tigriopus californicus, however, is devoid of major genetic components of the HIF pathway, and does not have respiratory gills or pigments – a molecule, such as hemoglobin in humans, that increases the ability to transport oxygen from the blood. Still, it is tolerant to extremely low levels of oxygen for at least 24 hours in its larval and adult stages.

A research from Oregon State University suggests that T. californicus can rely on other genes, those involved in cuticular reorganization and chitin metabolism, to successfully respond to hypoxic stress in their home in-between; cuticle refers to a layer secreted by and covering the epidermis, the outer layer of the skin, and the chitin forms an exoskeleton of a crustacean.

RNA sequencing of animals exposed to quasi-anoxic conditions – an extreme type of hypoxia – showed over 400 genes being expressed, with the genes for chitin metabolism and cuticle reorganization exhibiting consistent patterns of change during anoxia.

"This path is the potential solution of this small animal for low oxygen availability," said study co-author Felipe Barreto, assistant professor of integrative biology at OSU's Faculty of Sciences.

T. californicus has become an excellent model for studying physiological adaptations in the marine environment, said lead author of the study, Allie Graham, a postdoctoral researcher at Barreto's laboratory.

Last summer, Graham received a Postdoctoral Research Grant in Biology from the National Science Foundation to examine how marine organisms deal with stressful environmental conditions, especially hypoxia. Patterns and mechanisms for tolerating hypoxia of T. californicus were widely underestimated, she said.

"Hypoxia in ocean waters has rapidly increased in distribution, frequency, and severity," Graham said. "Some coastal ecosystems even reach anoxia levels seasonally. The low oxygen content makes life difficult for a wide range of organisms, and fish and crustaceans generally have the lowest levels of tolerance. "

T. californicus lives in pools that are mostly cooled by waves, unlike high tides, placing them and other pool dwellers under extreme environmental stress not only from low oxygen but also from fluctuations in salinity, acidity, and temperature.

"Without respiratory structures or pigment, T. californicus probably depends on cutaneous diffusion to exchange carbon dioxide for oxygen," Graham said. "Her physiology may explain how she can tolerate the loss of this crucial pathway of HIF and, in turn, co-opted other cellular stress response mechanisms to keep her oxygen levels stable.

"As someone who spent much of my doctoral work discussing the importance of the HIF pathway to animals in oxygen-limited environments, it certainly was a shock to not find these genes present in the genome of T. californicus," she added. . "Current literature discusses this pathway as if it were a given in all animals, which for vertebrates is crucial for the development of blood vessels and even plays a role in tumor biology. Therefore, the absence of these genes, the heart of the HIF pathway, is intriguing. "

The National Science Foundation and Oregon State University supported this research.

Hypoxia is often linked to the overgrowth of certain species of algae, which can cause oxygen depletion when they die, sink and decompose. Vast expanses of hypoxic water in the open ocean, known as dead zones, sometimes covering thousands of square miles, lead to the extinction of fish, corals, mollusks, and plants.

According to the National Oceanic and Atmospheric Administration, the number of American estuaries experiencing hypoxia has increased dramatically in the last decades, with more than half of them experiencing hypoxic conditions in any given year.

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