Environmental Oxygen is a Key Modulator of Development and Evolution: From Molecules to Ecology

Abstract

Oxygen is a key regulator of both development and homeostasis and a promising candidate to bridge the influence of the environment and the evolution of new traits. To clarify the various ways in which oxygen may modulate embryogenesis, its effects are reviewed at distinct organizational levels. First, the role of pathways that sense dioxygen levels and reactive oxygen species are reviewed. Then, the effects of microenvironmental oxygen on metabolism, stemness, and differentiation throughout embryogenesis are discussed. Last, the interplay between ecology and development are reexamined with a focus on the evolution of tetrapods, including during the emergence of a novel mechanism that shapes amniote limbs—interdigital cell death. Both genetic and environmental components work together during the formation of organisms, highlighting the importance of a multidisciplinary approach for understanding the evolution of new traits.

The tolerance to hypoxia is defined by a time-sensitive response of the gene regulatory network in sea urchin embryos

“…So even if the sea urchin embryos can survive 16 h of hypoxia, they will probably die in longer periods of low oxygen. Furthermore, in other organisms, ROS and hypoxia signaling regulate multiple developmental processes and, in some cases, these processes last throughout embryogenesis, which could make the embryos of these organisms even more sensitive to hypoxia than sea urchin embryos (Breus and Dickmeis, 2020;Coffman and Su, 2019;Cordeiro and Tanaka, 2020). In line with these alarming observations, lab experiments can show distinct and even opposing trends compared with experiments that are carried out in the field, owing to the increased and unexpected complexity of natural sites (Foo et al, 2020).…”

“…GRNs are the genomically encoded programs that control embryonic development, but the environmental conditions in which these GRNs operate can significantly affect their outcome (Beldade et al, 2011;Smith et al, 2018). Particularly, the use of hypoxia and redox gradients to control developmental processes in various phyla, might make the embryos more sensitive to low oxygen levels that are becoming more common in the ocean (Compernolle et al, 2003;Cordeiro and Tanaka, 2020;Dunwoodie, 2009;Semenza, 2012). The structure of the developmental GRN defines its function during environmental hypoxia and underlies the response and resilience to hypoxia during embryogenesis.…”

“…Recent studies indicate that oxygen loss in the oceans, termed deoxygenation, is more lethal to marine life than the direct effect of the rising temperatures or ocean acidification (Altieri et al, 2017;Breitburg et al, 2018;Hughes et al, 2020;Schmidtko et al, 2017;Vaquer-Sunyer and Duarte, 2008). The embryos of marine organisms could be highly sensitive to deoxygenation, especially embryos that use endogenous hypoxia and redox gradients as morphogens to guide the activation of gene regulatory networks (GRNs) during normal development (Chang et al, 2017;Coffman and Su, 2019;Cordeiro and Tanaka, 2020;Dunwoodie, 2009;Lendahl et al, 2009). Deciphering the structure and function of developmental GRNs that are activated by hypoxia and redox morphogens is key to understanding this fundamental regulatory mechanism as well as to assessing the expected effect of ocean deoxygenation on marine embryos.…”