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Adaptation to Deep-Sea Chemosynthetic Environments As Revealed by Mussel Genomes

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Adaptation to Deep-Sea Chemosynthetic Environments As Revealed by Mussel Genomes ARTICLES PUBLISHED: 3 APRIL 2017 | VOLUME: 1 | ARTICLE NUMBER: 0121 Adaptation to deep-sea chemosynthetic environments as revealed by mussel genomes Jin Sun1, 2, Yu Zhang3, Ting Xu2, Yang Zhang4, Huawei Mu2, Yanjie Zhang2, Yi Lan1, Christopher J. Fields5, Jerome Ho Lam Hui6, Weipeng Zhang1, Runsheng Li2, Wenyan Nong6, Fiona Ka Man Cheung6, Jian-Wen Qiu2* and Pei-Yuan Qian1, 7* Hydrothermal vents and methane seeps are extreme deep-sea ecosystems that support dense populations of specialized macro benthos such as mussels. But the lack of genome information hinders the understanding of the adaptation of these ani- mals to such inhospitable environments. Here we report the genomes of a deep-sea vent/seep mussel (Bathymodiolus plati- frons) and a shallow-water mussel (Modiolus philippinarum). Phylogenetic analysis shows that these mussel species diverged approximately 110.4 million years ago. Many gene families, especially those for stabilizing protein structures and removing toxic substances from cells, are highly expanded in B. platifrons, indicating adaptation to extreme environmental conditions. The innate immune system of B. platifrons is considerably more complex than that of other lophotrochozoan species, including M. philippinarum, with substantial expansion and high expression levels of gene families that are related to immune recognition, endocytosis and caspase-mediated apoptosis in the gill, revealing presumed genetic adaptation of the deep-sea mussel to the presence of its chemoautotrophic endosymbionts. A follow-up metaproteomic analysis of the gill of B. platifrons shows metha- notrophy, assimilatory sulfate reduction and ammonia metabolic pathways in the symbionts, providing energy and nutrients, which allow the host to thrive. Our study of the genomic composition allowing symbiosis in extremophile molluscs gives wider insights into the mechanisms of symbiosis in other organisms such as deep-sea tubeworms and giant clams. he environment of deep-sea hydrothermal vents and methane (1.64 Gb) was smaller than that of M. philippinarum (2.38 Gb), seeps is characterized by darkness, lack of photosynthesis- mainly because it has fewer repeats, particularly the Helitron- Tderived nutrients, high hydrostatic pressure, variable tem- transposable elements and unclassified repeats that together contrib- peratures and high concentrations of heavy metals and other toxic uted a 707 Mb difference between the two genomes (Supplementary 1,2 substances . Despite this hostile environment, these ecosystems Note 9). The N50 value (the shortest sequence length at 50% of the support dense populations of macrobenthos which, with the help genome size) of the B. platifrons scaffolds and contigs was 343.4 Kb of chemoautotrophic endosymbionts, are fuelled by simple reduced and 13.2 Kb, respectively; and the N50 value of the M. philippinarum molecules such as methane and hydrogen sulfide1–3. Studying vent scaffolds and contigs was 100.2 Kb and 19.7 Kb, respectively. The and seep organisms may answer fundamental questions about their deep-sea and shallow-water mussel genome contained 96.3% and origin and adaptation to the extreme environments1,4. Deep-sea 93.7% complete and partial universal single-copy metazoan ortholo- mussels (Mytilidae, Bathymodiolinae) often dominate at hydro- gous genes, respectively, indicating the completeness of the assembly thermal vents and cold seeps around the world. Owing to their and gene models (Supplementary Note 6). As with other bilateri- ecological importance and remarkable biological characteristics, ans, the two mussel genomes contained all the expected Hox and including their ability to survive an extended period under atmo- ParaHox genes, as well as similar numbers of microRNAs, again sug- spheric pressure5, they are a recognized model for studies of sym- gesting that the assemblies encapsulate a nearly complete representa- biosis6, immunity7, adaptation to abiotic stress8, ecotoxicology9 tion of genic information (Supplementary Note 13 and 14). Although and biogeography10. the gills of B. platifrons contain endosymbiotic methane-oxidizing bacteria (MOB)11, the host scaffolds did not contain bacterial nucle- Results and discussion otide sequences, showing a lack of horizontal gene transfer from the We sequenced the genomes of both B. platifrons Hashimoto and symbiont. B. platifrons has a lower rate of heterozygosity compared Okutani, 1994 (a deep-sea mussel, Fig. 1a) and M. philippinarum to the other three bivalves with a sequenced genome (Supplementary (Hanley, 1843) (a shallow-water mussel, Fig. 1b) in the family Fig. 3a), potentially owing to recurrent population bottlenecks as a Mytilidae using a whole-genome shotgun approach and compared result of population extinction and re-colonization12. their features (Supplementary Note 1). Both assembled genomes were The B. platifrons genome had 33,584 gene models, 86.2% of which highly repetitive (Supplementary Fig. 2). The genome of B. platifrons had transcriptome support, based on transcriptome data from three 1Division of Life Science, Hong Kong University of Science and Technology, Hong Kong, China. 2Department of Biology, Hong Kong Baptist University, Hong Kong, China. 3Shenzhen Key Laboratory of Marine Bioresource and Eco-Environmental Science, College of Life Science, Shenzhen University, Shenzhen, China. 4Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China. 5High Performance Computing in Biology, Roy J. Carver Biotechnology Centre, University of Illinois at Urbana–Champaign, Urbana, Illinois 61801, USA. 6Simon F. S. Li Marine Science Laboratory, School of Life Sciences, Centre for Soybean Research, Partner State Key Laboratory of Agrobiotechnology, the Chinese University of Hong Kong, Hong Kong, China. 7HKUST-CAS Joint Laboratory, Sanya Institute of Deep Sea Science and Engineering, Sanya 572000, China. *e-mail: [email protected]; [email protected] NATURE ECOLOGY & EVOLUTION 1, 0121 (2017) | DOI: 10.1038/s41559-017-0121 | www.nature.com/natecolevol 1 © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. ARTICLES NatURE ECOLOGY & EVOLUTION a b c Helobdella robusta d Pinctada fucata Capitella teleta Crassostrea gigas Lingula anatina Modiolus philippinarum Octopus bimaculoides Cephalopoda 94 Bathymodiolus platifrons 100 Lottia gigantea 100 100 Bathymodiolus azoricus Mytilidae 100 100 Biomphalaria glabrata Gastropoda 100 Aplysia californica 100 Perna viridis 100 100 Modiolus philippinarum Limnoperna fortunei Bathymodiolus platifrons 98 Mytilus coruscus Bivalvia 100 100 0.05 Crassostrea gigas Mytilus edulis 100 Pinctada fucata 0.01 100 Mytilus galloprovincialis Figure 1 | Shell morphology and phylogenetic positions of B. platifrons and M. philippinarum. a,b, Shell of the deep-sea mussel B. platifrons (a, 10.7 cm) and shallow-water mussel M. philippinarum (b, 6.5 cm). c, Phylogenetic tree of 11 lophotrochozoan species based on genome data; the value of bootstrap support is shown at each node. The scale bar indicates 0.05 expected substitutions per site. d, Phylogenetic tree of Mytilidae based on transcriptome data from representative genera/species. The scale bar indicates 0.01 changes per site. tissues in a previous study13, and our new transcriptome data from Among the most numerously expanded gene families in three additional tissues; whereas the M. philippinarum genome B. platifrons are the HSP70 family (179 proteins) and the ABC had 36,549 gene models, 86.0% of which had transcriptome sup- transporters (393 proteins). HSP70 is important for protein folding, port, based on our new transcriptome data from five tissues and thus high expression of these genes in the gill (Supplementary (Supplementary Note 5). A total of 5,527 B. platifrons gene models were Fig. 15) could indicate their active response to stresses such as validated by shotgun proteomics using gill samples (false discovery changing temperature, pH and hypoxia. However, because it took rate (FDR) < 0.01), and the gene-expression level correlated approximately three hours from the sample collection to preserva- well (P < 1 × 10−5) with their corresponding protein abundance tion, the high expression of some of the stress-related genes could (Supplementary Note 20). Comparisons among five molluscan also be caused by the stress experienced during the sampling and genomes revealed 6,883 shared protein domains and 474 protein transportation. Nevertheless, the expression level of HSP70 has domains unique to B. platifrons (Fig. 2a and Supplementary Table 14). been reported to positively correlate with the level of DNA-strand A phylogenetic tree constructed using 375 single-copy ortho- breakage in a deep-sea mussel16. Therefore, expansion of this gene logues from 11 lophotrochozoan species (Fig. 1c) and another tree family may provide additional genetic resources allowing deep-sea constructed using transcriptome sequences of representative mem- mussels to cope with abiotic stressors. ABC transporters are known bers of Mytilidae (Fig. 1d) showed that, within the genera used, to move toxic chemicals outside mussel gill epithelial cells17, form- Modiolus is the closest shallow-water relative of Bathymodiolus. ing the first line of defence against toxic chemicals in the vent/seep Using the lophotrochozoan tree as a reference, the time of diver- fluid. Many of the ABC transporters were highly expressed in the gence between B. platifrons and M. philippinarum was estimated
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