Abstract

The outbreak of invasive ascidianMolgula manhattensishas negatively affected marine and coastal ecosystems and caused huge economic loss in various industries such as aquaculture. In mariculture systems usually characterized by high ammonia nitrogen, the capacity ofM. manhattensisto defend against drastic ammonia elevation plays a crucial role in its survival and subsequent invasions. However, ammonia coping strategies and associated genes/proteins remain largely unknown. Here we investigated rhesus glycoproteins (Rh)-mediated ammonia transport by identifying all Rh proteins and exploring their mRNA expression regulations under ammonia stress. Three types of primitive Rh proteins were identified, and all contained conserved amino acid residues and functional domains. Ammonia stress largely suppressed the expression of immune-related genes, but rapidly induced the increased expression of Rh genes. Ammonia was converted into glutamine as indicated by the increased expression of glutamine synthetase gene, rather than urea as illustrated by the stable expression of arginase gene. Collectively,M. manhattensismitigates ammonia challenge by enhancing ammonia excretion through Rh channels and detoxifying ammonia into glutamine. Our results provide insights into the molecular mechanisms underlying high tolerance and invasion success to high ammonia environments by invasive ascidians.

Highlights

  • Specialty section: This article was submitted to Marine Biology, a section of the journal Frontiers in Marine ScienceReceived: 30 January 2021 Accepted: 16 March 2021 Published: 07 April 2021Citation: Chen Y, Huang X, Chen Y and Zhan A (2021) Ammonia Stress Coping Strategy in a Highly Invasive Ascidian

  • We reported that mRNA expression levels of the ITGAL and C3 were downregulated in M. manhattensis (Figure 7C), implying possible immune suppression caused by ammonia toxicity

  • Conserved amino acid residues and domains were identified in the three types of primitive rhesus glycoproteins (Rh) proteins of M. manhattensis, supplying molecular evidence to support their conserved functionality of ammonia transport

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Summary

Introduction

Specialty section: This article was submitted to Marine Biology, a section of the journal Frontiers in Marine ScienceReceived: 30 January 2021 Accepted: 16 March 2021 Published: 07 April 2021. The solitary tunicate Molgula manhattensis (DeKay, 1843), which is considered to be native to the northwest Atlantic Ocean, has successfully invaded coastal zones globally, such as the southwest coast of the Atlantic Ocean, the Mediterranean Sea, and the southwest, northwest, and northeast coasts of the Pacific Ocean in the past several decades (Lambert, 2003; Zvyagintsev et al, 2003; Hewitt et al, 2004; Haydar et al, 2011; Zhan et al, 2017; Chen et al, 2018; Fofonoff et al, 2018) Such high invasiveness is, at least partially, derived from its strong tolerance to various environmental stressors, including temperature, salinity, dissolved oxygen, and chemical pollution (Zvyagintsev et al, 2003; Pyo et al, 2012; Chen et al, 2018). In addition to its significantly negative ecological impacts along coasts, of particular concern is the enormous economic loss caused by M. manhattensis’ rapid establishment

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