The alternative oxidase (AOX) increases sulphide tolerance in the highly invasive marine invertebrateCiona intestinalis

Abstract

Ecological communities and biodiversity are shaped by both abiotic and biotic factors. This is well illustrated by extreme environments and invasive species. Besides naturally occurring sulphide-rich environments, global change can lead to an increase in hydrogen sulphide episodes that threaten many multicellular organisms. With the increase in the formation, size, and abundance of oxygen minimum zones and hypoxic environments, bacterial-associated sulphide production is favoured and as such hydrogen sulphide-rich environments increase subsequently. Many species are challenged by the inhibiting effect of sulphide on aerobic energy production via cytochrome c oxidase, ultimately causing the death of the organism. Interestingly, many protist, yeast, plant, and also animal species possess a sulphide-resistant alternative oxidase (AOX). In this study, we investigated whether AOX is functionally involved in the sulphide stress response of the highly invasive marine tunicate, Ciona intestinalis. At the LC50, the sulphide-induced reduction of developmental success was three times stronger in AOX knock-down embryos than in control embryos. Further, AOX mRNA levels were higher under sulphide than control conditions - and this effect increased during embryonic development. Together, we found that AOX is indeed functionally involved in the sulphide tolerance of Ciona embryos, hence, very likely contributing to its invasive potential; and that the response of AOX to sulphide seems to be controlled at the transcriptional level. We suggest that AOX-possessing species play an important role in shaping marine ecological communities, and this importance may increase under ongoing global change.

Targeting the alternative oxidase (AOX) for human health and food security, a pharmaceutical and agrochemical target or a rescue mechanism?

“…Since vertebrates lost AOX from their genome during evolution, Ciona intestinalis is now the closest known relative to humans still expressing a functional AOX enzyme. Remarkably, AOXs in fungi and Ciona appear to facilitate similar stress responses as has been described for plants, namely the conversion of cellular energy, redox homeostasis, and the control of mitochondrial ROS content [ 27 , 30 , 31 ] ( Figure 1 ). This role in stress response makes AOX a valuable therapeutic target in both agriculture and environmental protection and possibly also in in human infectious diseases.…”

“…In addition to its wide distribution in plants and prokaryotes, AOX is present in phytopathogenic fungi such as Blumeria graminis [ 20 ], Magnaporthe grisea [ 20 , 21 ], Septoria tritici [ 22 ], Ustilago maydis [ 20 , 23 ], Sclerotinia sclerotiorum [ 24 , 25 ] and Botrytis cinerea [ 20 , 26 ] to name but a few. Other notable species expressing AOX include the invertebrate marine worms Arenicola marina [ 27 ] and Sipunculus nudus [ 28 ], the bivalve Genkendia demissa [ 9 ], the Pacific oyster Crassostrea gigas [ 9 ], and the sea squirt Ciona intestinalis [ 29 , 30 ]. Since vertebrates lost AOX from their genome during evolution, Ciona intestinalis is now the closest known relative to humans still expressing a functional AOX enzyme.…”

Preference for and resistance to a toxic sulfur volatile opens up a unique niche inDrosophila busckii

“…Next, we aimed to demonstrate the involvement of COX in governing these tolerance phenotypes. Many animals exposed to extreme environments express an alternative oxidase (AOX), which functions similarly to COX but is reportedly resistant to known COX inhibitors [41][42][43] .…”