The coevolution of animals and oxygen in the Neoproterozoic

Author(s)

Flavia Ariany Belato Costa

• Document type: Doctoral Thesis
• Press: São Paulo.
• Institution: Universidade de São Paulo (USP). Instituto de Biociências (IBIOC/SB)
• Defense date: 2024-04-08

Examining board members

André Carrara Morandini; Ana Carolina Martins Junqueira; Emilio de Lanna Neto

• Advisor: André Carrara Morandini; Elisa Maria Costa e Silva de Paiva

Abstract

The relationship between oxygen and the emergence and diversification of animals is a topic that has been extensively debated by scientists over the decades. All animals currently described need oxygen to survive for at least part of their life cycle. Therefore, the transition from an anoxic to an oxygenated planet is considered by many authors as a prerequisite for the emergence and diversification of animals. However, our understanding of the correlation between environmental factors and evolutionary novelties remains limited. Although it is accepted that the Neoproterozoic oceans were habitats with low dissolved oxygen levels, we know little about the respiratory physiology of early animals adapted to live in those environments. To understand the physiology of the first metazoans, experimental and bioinformatic approaches were used here and revealed the divergence time of crucial metabolic pathways, and possible physiological adaptations of early animals to hypoxic conditions. Molecular dating of genes involved in oxygen metabolism and regulation, such as the Krebs cycle enzyme, Isocitrate Dehydrogenase (IDH), and the master-regulator of oxygen homeostasis, the hypoxia-inducible factor (HIF) suggests a pre-Cryogenian emergence of animals in low-oxygen conditions. Considering that, to understand how modern animals respond to low oxygen levels can also shed light on aspects of their ancestors\' physiology. To do so, the demosponge Hymeniacidon heliophila was considered as a modern analog and was submitted to the Neoproterozoic oceanic conditions in simulation chambers. Differential gene expression analysis showed that both oxygenated conditions and anoxia trigger the same physiological and molecular stress responses in sponges, suggesting a better adaptation to hypoxia. The results also suggest that although the first metazoans most likely did not have the HIF pathway as an oxygen-sensing mechanism, they probably used other means for that, such as the sulfide-removal pathway. The overexpression of genes related to glycolysis and the remodeling of the aquiferous system under oxidative stress suggests a possible ancestral role of these mechanisms in the first animals. Results presented here reveal possible physiological adaptations that may have been advantageous to early animals and contribute to our understanding of the intimate relationship between oxygen and metazoans diversification throughout the evolution of life. (AU)

• FAPESP's process: 19/18051-7 - Physiological, morphological and developmental responses of modern metazoans under the Neoproterozoic oceanic conditions
• Grantee: Flávia Ariany Belato Costa
• Support Opportunities: Scholarships in Brazil - Doctorate