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5. Distinct genomic routes underlie transitions to specialised symbiotic lifestyles in deep-sea annelid worms

Author

Moggioli, Giacomo, Panossian, Balig, Sun, Yanan, Thiel, Daniel, Martín-Zamora, Francisco M, Tran, Martin, Clifford, Alexander M, Goffredi, Shana K, Rimskaya-Korsakova, Nadezhda, Jékely, Gáspár, Tresguerres, Martin, Qian, Pei-Yuan, Qiu, Jian-Wen, Rouse, Greg W, Henry, Lee M, and Martín-Durán, José M

Subjects
Genetics, Nutrition, Animals, Symbiosis, Annelida, Polychaeta, Genome, Genomics, Phylogeny
Abstract

Bacterial symbioses allow annelids to colonise extreme ecological niches, such as hydrothermal vents and whale falls. Yet, the genetic principles sustaining these symbioses remain unclear. Here, we show that different genomic adaptations underpin the symbioses of phylogenetically related annelids with distinct nutritional strategies. Genome compaction and extensive gene losses distinguish the heterotrophic symbiosis of the bone-eating worm Osedax frankpressi from the chemoautotrophic symbiosis of deep-sea Vestimentifera. Osedax's endosymbionts complement many of the host's metabolic deficiencies, including the loss of pathways to recycle nitrogen and synthesise some amino acids. Osedax's endosymbionts possess the glyoxylate cycle, which could allow more efficient catabolism of bone-derived nutrients and the production of carbohydrates from fatty acids. Unlike in most Vestimentifera, innate immunity genes are reduced in O. frankpressi, which, however, has an expansion of matrix metalloproteases to digest collagen. Our study supports that distinct nutritional interactions influence host genome evolution differently in highly specialised symbioses.

Published
2023

13. Cold Seep Macrofauna

Author

Li, Yi-Xuan, Sun, Yanan, Lin, Yi-Tao, Xu, Ting, Ip, Jack Chi Ho, Qiu, Jian-Wen, Chen, Duofu, editor, and Feng, Dong, editor

Published
2023
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21. Signatures of Divergence, Invasiveness, and Terrestrialization Revealed by Four Apple Snail Genomes.

Author

Sun, Jin, Mu, Huawei, Ip, Jack, Li, Runsheng, Xu, Ting, Accorsi, Alice, Sánchez Alvarado, Alejandro, Ross, Eric, Lan, Yi, Sun, Yanan, Castro-Vazquez, Alfredo, Vega, Israel, Heras, Horacio, Ituarte, Santiago, Van Bocxlaer, Bert, Hayes, Kenneth, Cowie, Robert, Zhao, Zhongying, Zhang, Yu, Qian, Pei-Yuan, and Qiu, Jian-Wen

Subjects
Hox genes, gastropod, gene duplication, genomics, interchromosome rearrangement, mollusc, Adaptation, Biological, Animals, Genes, Homeobox, Genome, Introduced Species, Karyotype, Multigene Family, Oviposition, Phylogeny, Snails
Abstract

The family Ampullariidae includes both aquatic and amphibious apple snails. They are an emerging model for evolutionary studies due to the high diversity, ancient history, and wide geographical distribution. Insight into drivers of ampullariid evolution is hampered, however, by the lack of genomic resources. Here, we report the genomes of four ampullariids spanning the Old World (Lanistes nyassanus) and New World (Pomacea canaliculata, P. maculata, and Marisa cornuarietis) clades. The ampullariid genomes have conserved ancient bilaterial karyotype features and a novel Hox gene cluster rearrangement, making them valuable in comparative genomic studies. They have expanded gene families related to environmental sensing and cellulose digestion, which may have facilitated some ampullarids to become notorious invasive pests. In the amphibious Pomacea, novel acquisition of an egg neurotoxin and a protein for making the calcareous eggshell may have been key adaptations enabling their transition from underwater to terrestrial egg deposition.

Published
2019

37. Phylogenomic analyses reveal a single deep-water colonisation in Patellogastropoda

Author

Qi, Ying, Zhong, Zhaoyan, Liu, Xu, He, Xing, Zhou, Yadong, Zhang, Lili, Chen, Chong, Linse, Katrin, Qiu, Jian-Wen, Sun, Jin, Qi, Ying, Zhong, Zhaoyan, Liu, Xu, He, Xing, Zhou, Yadong, Zhang, Lili, Chen, Chong, Linse, Katrin, Qiu, Jian-Wen, and Sun, Jin

Abstract

Patellogastropoda, the true limpets, is a major group of gastropods widely distributed in marine habitats from the intertidal to deep sea. Though important for understanding their evolutionary radiation, the phylogenetic relationships among the patellogastropod families have always been challenging to reconstruct, with contradictory results likely due to insufficient sampling. Here, we obtained mitogenomic and phylogenomic data (transcriptomic or genomic) from six species representing the three predominantly deep-water patellogastropod families: Lepetidae, Neolepetopsidae, and Pectinodontidae. By using various phylogenetic methods, we show that mitogenome phylogeny recovers monophyly of eight families in most of the trees, though the relationships among families remain contentious. Meanwhile, a more robust family-level topology consistent with morphology was achieved by phylogenomics. This also reveals that these mainly deep-water families are monophyletic, suggesting a single colonisation of the deep water around the Jurassic. We also found a lack of significant correlation between genome size and habitat depth, despite some deep-water species exhibiting larger genome sizes. Our phylogenomic tree provides a stable phylogenetic backbone for Patellogastropoda that includes seven of the nine recognized families and paves the way for future evolutionary analyses in this major group of molluscs.

Published
2024

38. Genetic divergence and migration patterns of a galatheoid squat lobster highlight the need for deep-sea conservation

Author

Xu, Ting, Chai, Xia, Chen, Chong, Watanabe, Hiromi Kayama, Sun, Jin, Xiao, Yao, Wang, Yan, Chen, Junlin, Qiu, Jian-Wen, Qian, Peiyuan, Xu, Ting, Chai, Xia, Chen, Chong, Watanabe, Hiromi Kayama, Sun, Jin, Xiao, Yao, Wang, Yan, Chen, Junlin, Qiu, Jian-Wen, and Qian, Peiyuan

Abstract

Information on genetic divergence and migration patterns of vent- and seep-endemic macrobenthos can help delimit biogeographical provinces and provide scientific guidelines for deep-sea conservation under the growing threats of anthropogenic disturbances. Nevertheless, related studies are still scarce, impeding the informed conservation of these hotspots of deep-sea biodiversity. To bridge this knowledge gap, we conducted a population connectivity study on the galatheoid squat lobster Shinkaia crosnieri - a deep-sea foundation species widely distributed in vent and seep ecosystems in the Northwest Pacific. With the application of an interdisciplinary methodology involving population genomics and oceanographic approaches, we unveiled two semi-isolated lineages of S. crosnieri with limited and asymmetrical gene flow potentially shaped by the geographic settings, habitat types, and ocean currents - one comprising vent populations in the Okinawa Trough, with those inhabiting the southern trough area likely serving as the source; the other being the Jiaolong (JR) seep population in the South China Sea. The latter might have recently experienced a pronounced demographic contraction and exhibited genetic introgression from the Okinawa Trough lineage, potentially mediated by the intrusion of the North Pacific Intermediate Water. We then compared the biogeographic patterns between S. crosnieri and two other representative and co-occurring vent- and seep-endemic species using published data. Based on their biogeographical subdivisions and source-sink dynamics, we highlighted the southern Okinawa Trough vents and the JR seep warrant imperative conservation efforts to sustain the deep-sea biodiversity in the Northwest Pacific.

Published
2024

39. Scallop-bacteria symbiosis from the deep sea reveals strong genomic coupling in the absence of cellular integration

Author

Lin, Yi-Tao, Ip, Jack Chi-Ho, He, Xing, Gao, Zhao-Ming, Perez, Maeva, Xu, Ting, Sun, Jin, Qian, Peiyuan, Qiu, Jian-Wen, Lin, Yi-Tao, Ip, Jack Chi-Ho, He, Xing, Gao, Zhao-Ming, Perez, Maeva, Xu, Ting, Sun, Jin, Qian, Peiyuan, and Qiu, Jian-Wen

Abstract

Previous studies have revealed tight metabolic complementarity between bivalves and their endosymbiotic chemosynthetic bacteria, but little is known about their interactions with ectosymbionts. Our analysis of the ectosymbiosis between a deep-sea scallop (Catillopecten margaritatus) and a gammaproteobacterium showed that bivalves could be highly interdependent with their ectosymbionts as well. Our microscopic observation revealed abundant sulfur-oxidizing bacteria (SOB) on the surfaces of the gill epithelial cells. Microbial 16S rRNA gene amplicon sequencing of the gill tissues showed the dominance of the SOB. An analysis of the SOB genome showed that it is substantially smaller than its free-living relatives and has lost cellular components required for free-living. Genomic and transcriptomic analyses showed that this ectosymbiont relies on rhodanese-like proteins and SOX multienzyme complex for energy generation, mainly on the Calvin–Benson–Bassham (CBB) cycle and peripherally on a phosphoenolpyruvate carboxylase for carbon assimilation. Besides, the symbiont encodes an incomplete tricarboxylic acid (TCA) cycle. Observation of the scallop’s digestive gland and its nitrogen metabolism pathways indicates it does not fully rely on the ectosymbiont for nutrition. Analysis of the host’s gene expression provided evidence that it could offer intermediates for the ectosymbiont to complete its TCA cycle and some amino acid synthesis pathways using exosomes, and its phagosomes, endosomes, and lysosomes might be involved in harvesting nutrients from the symbionts. Overall, our study prompts us to rethink the intimacy between the hosts and ectosymbionts in Bivalvia and the evolution of chemosymbiosis in general.

Published
2024

40. One becomes three: An integrative morphological and molecular analysis of the windowpane oyster Placuna (Bivalvia: Pectinida) reveals new species.

Author

Lin, Yi‐Tao, Li, Yi‐Xuan, Loke, Hai‐Xin, Han, Xiao, and Qiu, Jian‐Wen

Subjects
TERRITORIAL waters, MARINE animals, SPECIES diversity, BIVALVES, OYSTERS
Abstract

For decades, many marine animals have been considered to exhibit cosmopolitan or transoceanic distribution. This situation is prevalent in Asia, where many species were collected and named by American or European experts in the 1700s to early 1900s. Using the windowpane oysters Placuna—a small genus of bivalves with five recognized species—we show that careful analysis is required to reassess the validity of these species. Currently, only two species of Placuna (P. placenta and P. ephippium) widely reported in the Indo‐Pacific region have been recorded from Chinese coastal waters. Here, we described two new species of Placuna from China. Placuna vitream sp. nov. can be distinguished from P. placenta by its larger ridge angle. Phylogenetic analysis using five gene fragments fully supported that P. vitream sp. nov. is a sister to the specimen from Singapore identified as P. placenta and more distant from other Placuna species with available molecular data. Besides, based on subfossil shells, we describe Placuna aestuaria sp. nov. that differs from its congeneric species by its broad hinge, medium ridge angle, and nearly straight ridges. Finally, we suggest a combination of hinge structure and ridge angle that can be used for identifying Placuna species and preparing a key to this genus. Our findings of two new species expand the diversity of Placuna and prompt reassessment of the many presumably widely distributed marine species in Asia. [ABSTRACT FROM AUTHOR]

Published
2024
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43. Insights from an Integrated View of the Biology of Apple Snails (Caenogastropoda: Ampullariidae)

Author

Hayes, Kenneth A, Burks, Romi L, Castro-Vazquez, Alfredo, Darby, Philip C, Heras, Horacio, Martín, Pablo R, Qiu, Jian-Wen, Thiengo, Silvana, Vega, Israel A., Wada, Takashi, Yusa, Yoichi, Burela, Silvana, Cadierno, M Pilar, Cueto, Juan A, Dellagnola, Federico A, Dreon, Marcos S, Frassa, M Victoria, Giraud-Billoud, Maximiliano, Godoy, Martín S, Ituarte, Santiago, Koch, Eduardo, Matsukura, Keiichiro, Pasquevich, M Yanina, Rodriguez, Cristian, Saveanu, Lucía, Seuffert, Maria E, Strong, Ellen E, Sun, Jin, Tamburi, Nicolás E, Tiecher, María J, Turner, Richard L., Valentine-Darby, Patricia L., Cowie, Robert H., and BioStor

Published
2015

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