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Pyropia Yezoensis Genome Reveals Diverse Mechanisms of Carbon Acquisition in the Intertidal Environment

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Pyropia Yezoensis Genome Reveals Diverse Mechanisms of Carbon Acquisition in the Intertidal Environment ARTICLE https://doi.org/10.1038/s41467-020-17689-1 OPEN Pyropia yezoensis genome reveals diverse mechanisms of carbon acquisition in the intertidal environment Dongmei Wang 1,2,9, Xinzi Yu1,2,9, Kuipeng Xu1,2,9, Guiqi Bi1,2,9, Min Cao1,2,9, Ehud Zelzion3, Chunxiang Fu4, Peipei Sun1,2, Yang Liu1,2, Fanna Kong1,2, Guoying Du1,2, Xianghai Tang1,2, Ruijuan Yang4, Junhao Wang1,2, Lei Tang1,2, Lu Wang 1,2, Yingjun Zhao1,2, Yuan Ge1,2, Yunyun Zhuang5, Zhaolan Mo6, Yu Chen1,2, Tian Gao1,2, ✉ Xiaowei Guan1,2, Rui Chen1,2, Weihua Qu 1,2, Bin Sun1,2, Debashish Bhattacharya 3 & ✉ Yunxiang Mao 1,7,8 1234567890():,; 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 het- eromorphic 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. 1 Key Laboratory of Marine Genetics and Breeding (OUC), Ministry of Education, 266100 Qingdao, China. 2 College of Marine Life Sciences, Ocean University of China, 266100 Qingdao, China. 3 Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, NJ 08901, USA. 4 Shandong Provincial Key Laboratory of Energy Genetics, Key Laboratory of Biofuels, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, 266101 Qingdao, China. 5 Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, 266100 Qingdao, China. 6 Key Laboratory of Maricultural Organism Disease Control, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, 266071 Qingdao, China. 7 Key Laboratory of Utilization and Conservation for Tropical Marine Bioresources (Hainan Tropical Ocean University), Ministry of Education, 572022 Sanya, China. 8 The Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, 266237 Qingdao, China. 9These authors contributed equally: Dongmei Wang, Xinzi Yu, Kuipeng Xu, Guiqi Bi, ✉ Min Cao. email: [email protected]; [email protected] NATURE COMMUNICATIONS | (2020) 11:4028 | https://doi.org/10.1038/s41467-020-17689-1 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-020-17689-1 he seaweed used most frequently to produce nori (sushi stress resistance. Photosynthesis in the thallus can recover rapidly wrap), Pyropia yezoensis, has a high nutritional value, from >80% water loss that results in the death of unwanted T – 7 including up to 25 30% protein by dry weight, vitamins (in epiphytes . This robustness facilitates commercial nori cultivation particular, B12), and oligosaccharides. The mariculture of nori in in the open sea. countries such as Korea, Japan, and China reaches an annual In contrast to P. haitanensis (another edible nori species), production of ca. 1.8 million tons1, making it, globally, one of the P. yezoensis is monecious. Mature thalli release sperm to fertilize most economically important marine crops. P. yezoensis is a carpospores (Fig. 1b, c). The resulting diploid zygotospores ger- member of the order Bangiales (family Bangiophyceae) in the red minate into the filamentous and branched conchocelis phase (the algae (Rhodophyta). Molecular phylogenetic studies, which sporophyte phase). The conchocelis burrows into the inner layers incorporate the fossil record, suggest that Bangiophyceae diverged of mollusk shells and lives within the calcareous matrix (Fig. 1d, from their sister group, the Florideophyceae, around 900 million e). The shell appears to provide protection from UV damage and 8 years ago (Mya). More limited phylogenomic data indicate that wave exposure . However, CO2 is scarce in the enclosed space the radiation of species within the Bangiophyceae occurred about that has reduced water exchange, which may limit growth of the ~250 Mya ago in the Permo-Carboniferous era, leading to for- conchocelis. Past work shows that increased atmospheric CO2 mation of the order Bangiales2,3. Species in Bangiales, for does not affect conchocelis photosynthetic performance, sug- instance, Pyropia spp. (e.g., P. yezoensis, P. haitanensis, Porphyra gesting the existence of an alternative carbon source6. Con- umbilicalis) and Bangia spp., typically have a life cycle char- chosporangia develop in mature conchocelis and release acterized by the alternation of heteromorphic generations that conchospores that attach to rocky substrata or P. yezoensis nets in live in distinctive habitats (Fig. 1). The edible, leafy thallus mariculture and develop into thalli, i.e., seedlings (Fig. 1f, g). (gametophyte) inhabits the upper intertidal zone of exposed Pyropia species appear to have evolved two distinct strategies coasts. These seaweeds attach to rocky substrata using a rhizoidal that are reflected in their life cycle: (1) the gametophyte thallus holdfast (Fig. 1a, g) and are exposed to air during low tide. Many utilizes atmospheric CO2 while living in a harsh environment and intertidal algae, including P. yezoensis, can utilize atmospheric (2) the sporophyte conchocelis is protected in the shell environ- 4–6 CO2 as the carbon source for photosynthesis . However, fre- ment but faces Ci limitation. The genome-wide impact of this quent emersion also leads to fluctuating environmental stresses, alternation of heteromorphic generations is poorly understood. such as extreme drought, high ultraviolet (UV) irradiance, and The genomes of P. umbilicalis and P. haitanensis have recently high temperature. For this reason, the P. yezoensis thallus, which been published9,10. Here we present the genome of P. yezoensis is capable of tolerating broad and extreme environmental stresses, and analyze Bangiales genome and transcriptomic data to gain is of interest as a model for studying molecular mechanisms of insights into the evolutionary mechanisms that allow these 1N 1N 1N a b g 2N 2N f c h 2N e d 2N Fig. 1 The life cycle of P. yezoensis showing the alternation of heteromorphic generations inhabiting distinctive niches. Ploidy was added as “1N” and “2N” in the upper left corner of each subgraph. a Gametophyte thalli adhered to rocks are exposed to air during low tide. b Carpospores and sperms form in mature thalli; c released zygotospores, showing one with a germ tube. d Purple patches on oyster shell are boring sporophyte conchocelis. e Swelling filamentous conchocelis that are going to produce conchosporangia. f Released conchospores. g Thallus seedling with a holdfast formed at the base. h P. yezoensis nets in mariculture farms. Scale bars in b, c, and e–g 50 μm. Asexual reproduction is not shown here. Microscope observation in b, c and e, g were repeated independently on multiple Pyropia samples (n > 10) showing similar morphology. 2 NATURE COMMUNICATIONS | (2020) 11:4028 | https://doi.org/10.1038/s41467-020-17689-1 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-020-17689-1 ARTICLE species to thrive in their stressful habitats vis-à-vis their transcribed genes. Gam-specifically transcribed genes were dimorphic life cycle. defined in the same way in the opposite direction. Genes with FPKM > 5 in both generations and fold change <10 were Results considered to be constitutively expressed. Because desiccation is one of the most important environmental stresses faced by Genome assembly. Assembly of the P. yezoensis genome using P. yezoensis thalli in the intertidal zone, we studied gene PacBio long-read sequencing data followed by removal of bac- expression patterns during a time course of desiccation and terial contaminant sequences resulted in 660 contigs with N50 = rehydration. In this regard, SOD catalyzes the dismutation of two 340.8 kbp (Supplementary Tables 1 and 2; Supplementary Figs. 1 molecules of the superoxide radical into one molecule of oxygen and 2). The genome size was estimated to be ca. 108 Mbp, which and one molecule of hydrogen peroxide (H O ), which can be is bigger than P. umbilicalis albeit comparable to the flor- 2 2 degraded into water and oxygen in the presence of catalase. Thus ideophyte Chondrus crispus. Hi-C and BioNano data linked the the antioxidant activity of SODs is of particular importance to the contigs into three scaffolds, S1 = 29.4 Mbp, S2 = 34.3 Mbp, and amelioration of cell damage induced by reactive oxygen species S3 = 43.6 Mbp, equivalent to the three chromosomes observed in (ROS) and maintenance of cell homeostasis. In plants, the SOD haploid P. yezoensis11 (Supplementary Tables 1–3, Supplemen- family consists of three classes of metalloenzymes, Fe-SOD, Mn- tary Figs. 3 and 4). These scaffolds included 95% of the genome
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