Pyropia yezoensis genome reveals diverse mechanisms of carbon acquisition in the intertidal environment

Dongmei Wang,Junhao Wang,Yunyun Zhuang,Min Cao,Guoan Bi ,Zhaolan Mo,Yingjun Zhao,Ehud Zelzion,Kuipeng Xu,Lei Tang,Ran Yang ,Bin Sun,Peilong Sun ,Debashish Bhattacharya,Xiaowei Guan,Tian Gao,Xiufeng Tang ,Chunxiang Fu,Guoying Du,Yu Chen,Yang Liu,Xinzi Yu,Fanna Kong,Rui Chen,Weihua Qu,Lu Wang,Yuan Ge,Yunxiang Mao

doi:10.1038/s41467-020-17689-1

Abstract

Changes in atmospheric CO2 concentration have played a central role in algal and plant adaptation and evolution. The commercially important red algal genus, Pyropia (Bangiales) appears to have responded to inorganic carbon (Ci) availability by evolving alternating heteromorphic generations that occupy distinct habitats. The leafy gametophyte inhabits the intertidal zone that undergoes frequent emersion, whereas the sporophyte conchocelis bores into mollusk shells. Here, we analyze a high-quality genome assembly of Pyropia yezoensis to elucidate the interplay between Ci availability and life cycle evolution. We find horizontal gene transfers from bacteria and expansion of gene families (e.g. carbonic anhydrase, anti-oxidative related genes), many of which show gametophyte-specific expression or significant up-regulation in gametophyte in response to dehydration. In conchocelis, the release of HCO3- from shell promoted by carbonic anhydrase provides a source of Ci. This hypothesis is supported by the incorporation of 13C isotope by conchocelis when co-cultured with 13C-labeled CaCO3.

Highlights

Changes in atmospheric CO2 concentration have played a central role in algal and plant adaptation and evolution
Species in Bangiales, for instance, Pyropia spp. (e.g., P. yezoensis, P. haitanensis, Porphyra umbilicalis) and Bangia spp., typically have a life cycle characterized by the alternation of heteromorphic generations that live in distinctive habitats (Fig. 1)
Hi-C and BioNano data linked the contigs into three scaffolds, S1 = 29.4 Mbp, S2 = 34.3 Mbp, and S3 = 43.6 Mbp, equivalent to the three chromosomes observed in haploid P. yezoensis[11] (Supplementary Tables 1–3, Supplementary Figs. 3 and 4)

Summary

Introduction

Changes in atmospheric CO2 concentration have played a central role in algal and plant adaptation and evolution. The commercially important red algal genus, Pyropia (Bangiales) appears to have responded to inorganic carbon (Ci) availability by evolving alternating heteromorphic generations that occupy distinct habitats. The leafy gametophyte inhabits the intertidal zone that undergoes frequent emersion, whereas the sporophyte conchocelis bores into mollusk shells. (e.g., P. yezoensis, P. haitanensis, Porphyra umbilicalis) and Bangia spp., typically have a life cycle characterized by the alternation of heteromorphic generations that live in distinctive habitats (Fig. 1). Pyropia species appear to have evolved two distinct strategies that are reflected in their life cycle: (1) the gametophyte thallus utilizes atmospheric CO2 while living in a harsh environment and (2) the sporophyte conchocelis is protected in the shell environment but faces Ci limitation. F c h e d species to thrive in their stressful habitats vis-à-vis their dimorphic life cycle

Methods

Results

Conclusion