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Qiu, J.-W.

Publications and source records attributed to Qiu, J.-W..

9 recordsLinked to original sources

Life finds a way: Integrative phylogenomics resolves an overlooked bivalve order with chromosome fusion and mitochondrial translational-code evolution

Resolving deep phylogenetic relationships requires integrating multiple lines of evidence, as distinct evolutionary forces shape signals from different genomic markers. Here, we investigate the systematics of the controversial APPD lineage (Anomiidae, Placunidae, Plicatulidae, and, by inference, Dimyidae) within Pectinida sensu lato using phylogenomic, comparative genomic, transcriptomic, proteomic, and morphological approaches. Our analyses consistently recover APPD as a monophyletic lineage sister to Limida and Pectinoidea, divergent at [~]428 Mya. With three novel high-quality genomes, extensive progressive chromosomal fusions demonstrate a reduction in chromosome number of the APPD lineage (6-13), compared with an ancestral 20 molluscan linkage groups (MLGs). Accompanied by extensive intrachromosomal gene-order scrambling, we identify one functional centromere in Placuna vitream flanked by two vestigial centromeric remnants on a single chromosome, providing a potential resource for investigating centromere inactivation and neocentromere formation. Mitochondrial genomes of APPD lineage exhibit unprecedented plasticity in translational decoding: Pododesmus employs the invertebrate mitochondrial code; Heteranomia employs +1 translational frameshifting to bypass in-frame TAG codons, whereas in Anomia, Enigmonia, Placuna, and Plicatulidae, TAA is reassigned to tyrosine and confirmed by proteomic evidence, which supports mitochondrial frameshifting in APPD lineage and defines a novel translation table for bivalves. Integrating phylogenetic distinctiveness, deep divergence, extreme karyotypic restructuring, unique mitochondrial features, and morphological diagnosability, we elevate the APPD lineage into Anomiida ord. nov. This revision resolves long-standing uncertainties for Pectinida sensu stricto and Limida, and establishes the APPD lineage as a valuable system for investigating chromosome fusion, centromere evolution, codon reassignment, and translational recoding. ClassificationBiological Sciences; Evolution SIGNIFICANCE STATEMENTWe have re-examined a controversial group of marine bivalves (Anomiidae, Placunidae, Plicatulidae, and Dimyidae). Our integrative approach shows that these animals split from scallops and their relatives more than 428 million years ago and have undergone drastic chromosomal fusions that reduced their chromosome number from 20 to as few as 6. Additionally, some species evolved unusual ways of reading their mitochondrial genetic code, either reassigning the stop codon to tyrosine or using +1 translational frameshifting to skip stop signals. The combination of deep evolutionary time and genomic divergence warrants recognizing them as a new order, Anomiida ord. nov. This work, as a case study, demonstrates how chromosome fusion and genetic code variation contribute to invertebrate diversity.

evolutionary biology↗

Two routes to land: Genomic underpinnings of parallel aerial egg deposition in aquatic Old-World Pila and New-World Pomacea (Ampullariidae)

The parallel evolution of aerial oviposition in Old-World Pila and New-World Pomacea apple snails--diverged since the Gondwanan breakup yet convergently transitioning from aquatic to terrestrial egg deposition--offers a powerful model for probing genomic adaptations underpinning key evolutionary innovations. We generated chromosomal-level genomes of Pila celebensis and Pila pesmei, revealing a genus-specific doubling in genome size driven by transposable element expansions. Parallel chromosomal rearrangements linked to environmental sensing, stress responses, and metabolism were identified in both lineages. Gene family analyses uncovered parallel expansions in cellulases, immune genes, and environmental sensors, alongside convergent positive selection in aquaporins critical for aerial osmoregulation. Strikingly, proteomics of egg perivitelline fluid (PVF) highlighted parallel adaptations in the PV1 protein family, where increased hydrophobicity enhances desiccation resistance in aerially deposited eggs. Phylogenetic and structural evidence traced PV1s likely origin to horizontal gene transfer (HGT) from a virus in the Ampullariidae ancestor, with subsequent duplications enabling lineage-specific aerial adaptations. Despite distinct genomic trajectories, Pila and Pomacea demonstrate that parallel molecular evolution and HGT-driven innovation facilitated their convergent transition to terrestrial reproduction, providing unprecedented insights into the genomic architecture of adaptive convergence.

evolutionary biology↗

A multilamellar organelle for chemosymbiosis in an aplacophoran mollusc adapted to anoxic cold seep sediment

Symbiosis with chemoautotrophic bacteria has evolved in many animal lineages inhabiting reducing habitats such as hydrothermal vents, allowing these holobionts to thrive in dark biospheres1. In certain instances, the symbionts have become intracellular, residing within specialised bacteriocytes2. The integration of microbial symbionts with eukaryotic cells vary across known animals; however, no specialised organelle dedicated to chemosynthesis has been identified yet2. Here, we report a mode of symbiosis where sulphur-oxidising bacteria cultured within spherical multilamellar compartments (~12 m) in the cold-seep aplacophoran mollusc Chaetoderma shenloong. This organelle, which we name dracosphera, is ubiquitous within the hypertrophied and intricately reticulate digestive gland of C. shenloong, which has otherwise lost most of its gut. Given that the symbionts are strictly anaerobic and the host resides in anoxic sediments tens of centimetres below the surface, the dracosphera may serve to minimise oxygen diffusion to the bacteria, akin to mechanisms observed in microbial diazotrophs3 or termite hindguts4, as supported by our genomic and spatial transcriptomic analyses. Hypoxic conditions have been known to induce radical adaptations in meiofauna, exemplified by the acquisition of hydrogenosomes5. Our discovery of similarly exceptional adaptations in C. shenloong provides new insights into the evolution of such organelles also in larger animals.

microbiology↗

VEHoP: A Versatile, Easy-to-use, and Homology-based Phylogenomic pipeline accommodating diverse sequences

Phylogenomics has emerged as a transformative approach in systematics, conservation biology, and biomedicine, enabling the inference of evolutionary relationships by leveraging hundreds to thousands of genes from genomic or transcriptomic data. However, acquiring high-quality genomes and transcriptomes necessitates samples with intact DNA and RNA, substantial sequencing investments, and extensive bioinformatic processing, such as genome/transcriptome assembly and annotation. This challenge is particularly pronounced for rare or difficult-to-collect species, such as those inhabiting the deep sea, where only fragmented DNA reads are often available due to environmental degradation or suboptimal preservation conditions. To address these limitations, we introduce VEHoP (Versatile, Easy-to-use Homology-based Phylogenomic pipeline), a tool designed to infer protein-coding regions from diverse inputs, including raw reads (short and long), draft genomes, transcriptomes, and annotated genomes. VEHoP automates the generation of orthologous sequence alignments, concatenated matrices, and phylogenetic trees, streamlining phylogenomic analyses for researchers across disciplines. The tool aims to (1) expand taxonomic sampling by accommodating a wide range of input data types and (2) simplify phylogenomic workflows, making them accessible to researchers with varying levels of bioinformatic expertise. We evaluated VEHoPs performance using datasets from oysters, catfish, and insects, demonstrating its ability to produce robust phylogenetic trees with strong bootstrap support, outperforming assembly-free methods. Additionally, we applied VEHoP to reconstruct the phylogeny of the enigmatic deep-sea gastropod order Neomphalida, successfully resolving a well-supported phylogenetic backbone for this poorly understood group. VEHoP is freely available on GitHub (https://github.com/ylify/VEHoP), with dependencies easily installable via Bioconda.

bioinformatics↗

The hologenome of Osedax frankpressi reveals the genetic interplay for the symbiotic digestion of vertebrate bone

The marine annelid Osedax has evolved a unique heterotrophic symbiosis that allows it to feed exclusively on sunken bones. Yet, the genetic and physiological principles sustaining this symbiosis are poorly understood. Here we show that Osedax frankpressi has a small, AT-rich genome shaped by extensive gene loss. While the Oceanospirillales endosymbiont of Osedax is enriched in genes for carbohydrate and nitrogen metabolism, O. frankpressi has undergone genetic changes to accommodate bone digestion, including the expansion of matrix metalloproteases, and a loss of pathways to synthesize amino acids that are abundant in collagen. Unlike other symbioses, however, innate immunity genes required to acquire and control the endosymbionts are reduced in O. frankpressi. These findings reveal Osedax has evolved an alternative genomic toolkit to bacterial symbiosis where host-symbiont co-dependence has favoured genome simplicity in the host to exploit the nutritionally unbalanced diet of bones. TeaserGenome reduction and adaptations for collagen digestion underpin the symbiosis of Osedax worms to exploit decaying bones.

genomics↗

Dual symbiosis in the deep-sea hydrothermal vent snail Gigantopelta aegis revealed by its hologenome

Animals endemic to deep-sea hydrothermal vents often form obligatory relationships with bacterial symbionts, maintained by intricate host-symbiont interactions. Endosymbiosis with more than one symbiont is uncommon, and most genomic studies focusing on such dual symbiosis systems have not investigated the host and the symbionts to a similar depth simultaneously. Here, we report a novel dual symbiosis among the peltospirid snail Gigantopelta aegis and its two Gammaproteobacteria endosymbionts - one being a sulphur oxidiser and the other a methane oxidiser. We assembled high-quality genomes for all three parties of this holobiont, with a chromosome-level assembly for the snail host (1.15 Gb, N50 = 82 Mb, 15 pseudo-chromosomes). In-depth analyses of these genomes reveal an intimate mutualistic relationship with complementarity in nutrition and metabolic codependency, resulting in a system highly versatile in transportation and utilisation of chemical energy. Moreover, G. aegis has an enhanced immune capability that likely facilitates the possession of more than one type of symbiont. Comparisons with Chrysomallon squamiferum, another chemosymbiotic snail in the same family but only with one sulphur-oxidising endosymbiont, show that the two snails sulphur-oxidising endosymbionts are phylogenetically distant, agreeing with previous results that the two snails have evolved endosymbiosis independently and convergently. Notably, the same capabilities of biosynthesis of specific nutrition lacking in the host genome are shared by the two sulphur-oxidising endosymbionts of the two snail genera, which may be a key criterion in the selection of symbionts by the hosts.

genomics↗

Tripartite holobiont system in a vent snail broadens the concept of chemosymbiosis

Many animals inhabiting deep-sea vents are energetically dependent on chemosynthetic endosymbionts, but how such symbiont community interacts with host, and whether other nutritional sources are available to such animals remain unclear. To reveal the genomic basis of symbiosis in the vent snail Alviniconcha marisindica, we sequenced high-quality genomes of the host and gill campylobacterial endosymbionts, as well as metagenome of the gut microbiome. The gill endosymbiont has a streamlined genome for efficient chemoautotrophy, but also shows metabolic heterogeneity among populations. Inter- and intra-host variabilities among endosymbiont populations indicate the host poses low selection on gill endosymbionts. Virulence factors and genomic plasticity of the endosymbiont provide advantages for cooperating with host immunity to maintain mutualism and thriving in changing environments. In addition to endosymbiosis, the gut and its microbiome expand the holobionts utilisation of energy sources. Host-microbiota mutualism contributes to a highly flexible holobiont that can excel in various extreme environments.

ecology↗

A highly stable, nondigestible lectin from Pomacea diffusa unveils clade-related protection systems in apple snail eggs

The acquisition of egg protection is vital for species survival. Poisonous eggs from Pomacea apple snails have defensive macromolecules for protection. Here we isolated and characterized a novel lectin called PdPV1 that is massively accumulated in the eggs of Pomacea diffusa and seems part of its protective cocktail. The native protein, an oligomer of ca. 256 kDa, has high structural stability, withstanding 15 min boiling and denaturing by sodium dodecyl sulphate. It resists in vitro proteinase digestion and displays structural stability between pH 2.0-12.0 and up to 85 {degrees}C. These properties, as well as its subunit sequences, glycosylation pattern, presence of carotenoids, size, and global shape resemble those of its orthologs from other Pomacea. Further, like members of the canaliculata clade, PdPV1 is recovered unchanged in faeces of mice ingesting it, supporting an antinutritive defensive function. PdPV1 also displays a strong hemagglutinating activity specifically recognizing selected ganglioside motifs with high affinity. This activity is only shared with PsSC, a perivitelline from the same clade (bridgesii clade). As a whole, these results indicate that species in the genus Pomacea have diversified their eggs defences: Those from the bridgesii clade are protected mostly by non-digestible lectins that lower the nutritional value of eggs, in contrast with protection by neurotoxins of other Pomacea clades, indicating apple snail egg defensive strategies are clade-specific. The harsh gastrointestinal environment of predators would have favoured their appearance, extending by convergent evolution the presence of plant-like highly stable lectins, a strategy not reported in other animals. Summary statementAnalysis of key snail egg proteins shows evolutionary defensive trends associated with the phylogenetic position, extending by convergent evolution the presence of plant-like defensive strategies not reported in other animals

biochemistry↗

Exaptation of two ancient immune proteins into a new dimeric pore-forming toxin in snails

The Membrane Attack Complex-Perforin (MACPF) family is ubiquitously found in all kingdoms. They have diverse cellular roles but MACPF but pore-forming toxic function are very rare in animals. Here we present the structure of PmPV2, a MACPF toxin from the poisonous apple snail eggs, that can affect the digestive and nervous systems of potential predators. We report the three-dimensional structure of PmPV2, at 15 [A] resolution determined by negative stain electron microscopy (NS-EM) and its solution structure by small angle X-ray scattering (SAXS). We found that PV2s differ from nearly all MACPFs in two respects: it is a dimer in solution and protomers combine two immune proteins into an AB toxin. MACPF chain is linked by a single disulfide bond to a tachylectin chain, and two heterodimers are arranged head-to-tail by non-covalent forces in the native protein. MACPF domain is fused with a putative new Ct-accessory domain exclusive to invertebrates. Tachylectin is a six-bladed {beta}-propeller, similar to animal tectonins. We experimentally validated the predicted functions of both subunits and demonstrated for the first time that PV2s are true pore-forming toxins. The tachylectin ..B.. delivery subunit would bind to target membranes, and then its MACPF ..A.. toxic subunit disrupt lipid bilayers forming large pores altering the plasma membrane conductance. These results indicate that PV2s toxicity evolved by linking two immune proteins where their combined preexisting functions give rise to a new toxic entity with a novel role in defense against predation. This structure is an unparalleled example of protein exaptation.

biochemistry↗