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The Quagga Mussel Genome and the Evolution of Freshwater Tolerance

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The Quagga Mussel Genome and the Evolution of Freshwater Tolerance bioRxiv preprint doi: https://doi.org/10.1101/505305; this version posted December 23, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. The quagga mussel genome and the evolution of freshwater tolerance Andrew D. Calcino1, André Luiz de Oliveira1, Oleg Simakov2, Thomas Schwaha1, Elisabeth Zieger1, Tim Wollesen3 and Andreas Wanninger1 1Department of Integrative Zoology, University of Vienna, Austria. 2Department of Molecular Evolution and Development, University of Vienna, Austria. 3Developmental Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany ABSTRACT European freshwater dreissenid mussels evolved from marine ancestors during the Miocene approximately 30 million years ago and today include some of the most successful and destructive invasive invertebrate species of temperate freshwater environments. Here we sequenced the genome of the quagga mussel Dreis- sena rostriformis to identify evolutionary adaptations involved in embryonic osmoregulation. We found high gene expression levels of a novel subfamily of lophotrochozoan-specific aquaporin water channel, a vacuolar ATPase and a sodium/hydrogen exchanger during early cleavage, a period defined by the formation of inter- cellular fluid-filled ‘cleavage cavities’. Independent expansions of the lophotrochoaquaporin clade that coin- cide with at least five independent colonisation events of freshwater environments confirm their central role in freshwater adaptation. The pattern of repeated aquaporin expansion and the evolution of membrane-bound fluid-filled osmoregulatory structures in diverse taxa points to a fundamental principle guiding the evolution of freshwater tolerance that may provide a framework for future efforts towards invasive species control. Keywords: Dreissena rostriformis, quagga mussel, genome, osmoregulation, aquaporin, v-ATPase, Lopho- trochozoa, Mollusca, Bivalvia. MAIN TEXT Molluscs evolved in the ocean, yet today there are ap- perosmotic to their environment (9, 10). This differs proximately 5000 freshwater species worldwide origi- to marine and brackish water species which are com- nating from more than 40 independent colonisation monly osmoconformers (11). Due to their large surface events (1–3). While most freshwater mollusc species area to volume ratio, the issue of cellular osmoregula- are gastropods (ca. 4000 species, 2), several bivalves tion is expected to be particularly acute for the eggs (eg. Dreissena rostriformis, Dreissena polymorpha, Lim- and embryos of broadcast spawners such as the quagga noperna fortune and Corbicula fluminea) have proven mussel Dreissena rostriformis (Fig. 1; Supplementary to be highly successful and ecologically disruptive eco- note SM 1). The evolution of mechanisms by the quag- system engineers of colonised environments (4–7). ga mussel to withstand the harsh osmotic conditions of the freshwater environment during embryogenesis Bivalves have invaded freshwater habitats on at least may be a contributing factor to their evolutionary suc- 11 occasions (3, 8). Despite the independence of these cess and their ability to rapidly spread through newly events, a feature common to freshwater species is a colonised habitats. - body fluid osmolarity that is actively maintained hy bioRxiv preprint doi: https://doi.org/10.1101/505305; this version posted December 23, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. a b c Dreissena rostriformis Dreissena polymorpha Mya arenaria Glossus humanus d Arctica islandica Mercenaria campechiensis Rangia cuneata Cyrenoida floridana Corbicula fluminea IMPARIDENTIA Diplodonta sp Cycladicama cumingi Donacilla cornea Sphaerium corneum Cerastoderma edule Hiatella arctica Galeomma turtoni Lasea adansoni Lamychaena hains Phacoides pectinata Myochama anomiodes ANOMALODESMATA Lyonsia floridana Eucrassatella cumingii Astarte sulcata ARCHIHETERODONTA Cardites antiquata Margaritifera margaritifera Lampsilis cardium PALEOHETERODONTA Neotrigonia margaritacea Crassostrea gigas* Atrina rigida Pinctada fucata* Patinopecten yessoensis* Placopecten magellanicus Mytilus edulis Limnoperna fortunei* PTERIOMORPHA Bathymodiolus platifrons* Modiolus philippinarum* Arca noae Philobryidae sp. Neocardia sp. Yoldia limatula Ennucula tenuis PROTOBRANCHIA Solemya velum Chiton olivaceus Laevipilina hyalina Octopus vulgaris Lottia gigantea* Gadila tolmiei Greenland neomeniomorph .06 Figure 1. The quagga mussel, Dreissena rostriformis. (a) Quagga mussels form dense aggregations connected with strong byssal threads. Aggregates are often associated with other benthic species such as sponges. (b) Illustra- tion of a single quagga mussel demonstrating the distinct banding pattern of the shell and the dense clump of byssus threads that enables them to adhere to both natural and manufactured substrates. (c) Global distribution of the quagga mussel highlighting native (blue) and colonised (red) habitats. (d) Condensed phylogeny of Bivalvia (58) based on a supermatrix composed of 47 molluscan taxa covering 1,377 orthogroups. The quagga mussel is positioned amongst the Imparidentia. Species with sequenced genomes are marked with a *. All nodes possess support values equal to 1. To identify genetic signatures that have underpinned the non-redundant haploid assembly covers 1.24 Gb with a transition to freshwater environments, we sequenced, scaffold N50 of 131.4 kilobases. The difference of ~360 assembled and annotated the ~1.6 gigabase (Gb) ge- megabases between the assembled genome and the nome of the quagga mussel D. rostriformis (Supplemen- predicted genome size is most likely explained by the tary notes SM 1-2). High heterozygosity (~2.4%) and collapsing or reduction of highly repetitive regions, as repeat content of the genome (Supplementary note has been observed with other genome assemblies (16). Mapping of the paired end libraries back to the com- designed for dealing with these issues, which are com- pleted genome resulted in 94.5% realignment, con- monSM 3) to necessitated many wild-type an assembly non-inbred pipeline invertebrate specifically spe- cies (Supplementary note SM 4; 12–15). The resulting firming the integrity of the assembly. bioRxiv preprint doi: https://doi.org/10.1101/505305; this version posted December 23, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. Annotation of the assembly was performed through a wise diffuse across membranes, or to excrete excess combination of RNAseq-based transcriptome assem- blies, homology data and ab-inito methods, resulting in small solutes (eg. Na+, K+, Cl-) that would otherwise be - lostwater to thatthe environmentpasses into their must cells. be prevented Likewise, theor balanced efflux of els (Supplementary note SM 5). BUSCO analysis (v. 2.0, with uptake to avoid deteriorating osmotic conditions. 17the identification of 37,681 protein-coding gene mod An investigation of the genes encoding sodium, potas- sium, chloride and water transmembrane channels in gene) detected models could928 (94.9%) be annotated of the based 978 metazoan on homology single to Dreissena revealed an aquaporin, a vacuolar ATPase (v- publiccopy orthologues databases. Theseand in results total 32,708make the (85.8%) quagga of mus the- ATPase) subunit a and a sodium/hydrogen exchanger sel genome one of the most high quality and complete (NHE) that are highly expressed in Dreissena eggs and molluscan assemblies currently available and an im- early embryos (stages that lack distinct osmoregula- portant resource for metazoan genomics. tory organs) but not in those of the marine oyster Cras- sostrea gigas (Fig. 2a; Supplementary note SM6). In order to maintain a body osmolarity above that of the surrounding medium, organisms require mechanisms - to either prevent the influx of water that would other 1 Mma_129733_1 Color Key Eco_24500 Mma_5864_1 a b Mma_318_16 Mma_3061_2 Mma_318_20 0.99 Lca_3762_1 Unionid 1 −2 −1 0 1 2 Vli_2092_26 Eco_10030 Vli_2092_28 Row Z −Score 0.93 Vli_2092_29 Mma_318_18 Eco_44130 Gene.75921 Aquaporin Mma_5616_1 Mma_53530_1 Mma_86294_1 Nma_5305_2 Gene.85204 NK ATPase Vli_3608_16 Unionid 2 Vli_4458_5 Vli_3608_8 Gene.62031 NHE Lca_1121_1 Eco_3240 Eco_3358 Mma_21490_1 Gene.62284 v-ATPase sub I 0.98 1 Mma_15703_1 Vli_49754_1 Unionid 3 l Eco_27751 l r Mma_386_1 e 1 r 1 e e 3 e 2 e 4 r 2 r 5 r 4 r s 3 Eco_5301 r r r e er 1 0.95 egg r e e e er 3 er 2 Unionid 4 trula o Vli_1432_1 o o o g e s d g g h trula 1 h h h Vli_3889_4 elig trula 2 2-4 ce s 0.89 elig s v eli Mma_318_19 elig elig elig eli eli Ga a v a V v v v elig V V Eco_16040 g g tilise v 0.95 y 1 Vli_3889_3 y y r l Unionid 5 l l g r g ped e r r Vli_3889_1 ochop ochop ochop ochop f n ped r a n ped ped ped r r r Mma_3061_1 T Ea a n T T T Ea Ea a a a ped Dro_Gene_26518 mi U a mi Dpo_Gene_17765 m m 0.98 Dro_Gene_26517 Dreissena D-sh D-sh D-sh D-sh e D-sh 0.89 Dro_Gene_75921 t D-sh Swi Dpo_Gene_11343 Swi 0.97 La Mar_5380_1 1 C_12095_1 C_10103_2 0.88 C_10103_5 Corbicula C_9847_2 C_23001_1 Cgi_EKC35416_aqp 3.94 1 2 3 4 5 6 7 8 9 10 Cgi_EKC35418_aqp
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