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Francis, W. R.

Publications and source records attributed to Francis, W. R..

11 recordsLinked to original sources

Environmental DNA reveals hidden eukaryotic diversity and fine-scale community patterns across seascape areas in the Northern Red Sea

Understanding how reef-associated biodiversity responds to seascape features is essential for monitoring and conserving coral reef ecosystems. Environmental DNA (eDNA) from seawater provides access to benthopelagic eukaryotic diversity but its relationship with benthic structure remains poorly understood. We conducted simultaneous assessment of benthopelagic eDNA derived from near-reef seawater and benthic photoquadrat surveys across 12 coral reef sites in the northern Red Sea, spanning three seascape regions: the Gulf of Aqaba, nearshore Northern Red Sea (NRS), and offshore NRS. We examined whether spatial patterns in benthopelagic eDNA communities were structured across regions and whether variation in benthic cover explained differences in eDNA-derived assemblages obtained from water samples. Benthopelagic eDNA revealed fine-scale spatial structuring across regions but showed non-significant whole-community correlation with benthic composition. When examined by major taxonomic groups, taxon-specific relationships emerged, with some taxa (i.e., Micromonas sp.) showing increasing relative abundances in reefs characterized by lower benthic complexity. While traditional photoquadrat surveys captured 72 benthic sessile taxa including dominant benthic groups (e.g. hard corals and algae) across four eukaryotic phyla, benthopelagic eDNA documented a broader range of eukaryotic diversity, including planktonic, cryptic, and low abundant taxa spanning 35 phyla. Notably, eDNA detected cryptic organisms overlooked by visual surveys, such as the giant clam Tridacna sp., even where present but not recorded in photoquadrats. Our results demonstrate that benthopelagic eDNA and visual surveys provide complementary perspectives on reef biodiversity. Rather than serving as a direct proxy for benthic structure, benthopelagic eDNA captures spatial and taxonomic patterns that may be overlooked by visual transects, supporting its use in seascape-scale biodiversity assessments and conservation planning efforts in dynamic and understudied reef systems.

ecology↗

Genomic changes are varied across congeneric species pairs

Synteny, the shared arrangement of genes on chromosomes between related species, is a marker of shared ancestry, and synteny-breaking events can result in genomic incompatibilities between populations and ultimately lead to speciation events. Despite its pivotal role as a driver of speciation, the role of synteny breaks on speciation is poorly studied due to a lack of chromosome-level genome assemblies for a taxonomically broad sample of organisms. Here, using 22 congeneric animal genome pairs, we find a link between protein identity, microsynteny, and macrosynteny, but no evidence for a universal path of genomic change during divergence. We observed varied trajectories of synteny conservation relative to protein identity in non-model organisms, with many species pairs showing no karyotypic changes and others displaying large genomic rearrangements. This contrasts with previous studies on model organisms and indicates that the genomic changes preceding or resulting from speciation are likely very contextual between clades.

genomics↗

Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia

Deoxygenation can be fatal for many marine animals; however, some sponge species are tolerant of hypoxia and anoxia. Indeed, two sponge species, Eurypon sp. 2 and Hymeraphia stellifera, survive seasonal anoxia for months at a time. To understand their tolerance mechanisms, we performed differential gene expression analyses on the sponges, their mitochondria and their microbial symbionts under in situ conditions of normoxia, hypoxia and anoxia. Each species possessed a unique microbiome, but the microbiomes of each species were dominated by a species-specific Thaumarchaeon and a Gammaproteobacterium. Holobiont gene expression was species-and oxygen-level dependent, though there were some shared interspecific responses to deoxygenation. In general, few changes occurred in the expression of sponge metabolic genes as a function of oxygenation level, indicating that they may remain metabolically active under anoxia. However, ATP synthesis genes were significantly upregulated under hypoxia when compared to normoxia, and genes for DNA replication were downregulated. Mitochondrial gene expression was effectively unchanged under both hypoxia and anoxia. Nevertheless, both anoxia and hypoxia caused upregulation of heat shock proteins (HSPs), indicating cellular level adaptations to deoxygenation stress. A meta-analysis demonstrated that sponge transcriptional responses to anoxia were distinct from those displayed by other invertebrates while dormant, and the hypothesis of sponge dormancy under anoxia was not supported. Thaumarchaeota symbionts also upregulated stress response genes in hypoxia, while maintaining expression of oxygen-dependent metabolic pathways under hypoxia and anoxia. Gammaproteobacteria symbionts showed relatively few noteworthy changes in gene expression in response to anoxia but decreased metabolic gene expression in hypoxia. There was no clear evidence of upregulated anaerobic respiration in the transcriptomes of the sponge holobionts under anoxia or hypoxia. The tolerance of some sponges to prolonged anoxia warrants further investigation and could give them an advantage in future oceans following climate change as well as in ancient oceans when oxygen concentrations were lower than at present.

ecology↗

Metagenomic data for Halichondria panicea from Illumina and Nanopore sequencing and preliminary genome assemblies for the sponge and two microbial symbionts.

ObjectivesThese data were collected to generate a novel reference metagenome for the sponge Halichondria panicea and its microbiome for subsequent differential expression analyses. Data descriptionThese data include raw sequences from four separate sequencing runs of the metagenome of a single individual of Halichondria panicea - one Illumina MiSeq (2x300 bp, paired-end) run and three Oxford Nanopore Technologies (ONT) long-read sequencing runs, generating 53.8 and 7.42 Gbp respectively. Comparing assemblies of Illumina, ONT and an Illumina-ONT hybrid revealed the hybrid to be the best assembly, comprising 163 Mbp in 63,555 scaffolds (N50: 3,084). This assembly, however, was still highly fragmented and only contained 52% of core metazoan genes (with 77.9% partial genes), so it was also not complete. However, this sponge is an emerging model species for field and laboratory work, and there is considerable interest in genomic sequencing of this species. Although the resultant assemblies from the data presented here are suboptimal, this data note can inform future studies by providing an estimated genome size and coverage requirements for future sequencing, sharing additional data to potentially improve other suboptimal assemblies of this species, and outlining potential limitations and pitfalls of the combined Illumina and ONT approach to novel genome sequencing.

genomics↗

Bioluminescence and fluorescence of three sea pens in the north-west Mediterranean sea

Bioluminescence of Mediterranean sea pens has been known for a long time, but basic parameters such as the emission spectra are unknown. Here we examined bioluminescence in three species of Pennatulacea, Pennatula rubra, Pteroeides griseum, and Veretillum cynomorium. Following dark adaptation, all three species could easily be stimulated to produce green light. All species were also fluorescent, with bioluminescence being produced at the same sites as the fluorescence. The shape of the fluorescence spectra indicates the presence of a GFP closely associated with light production, as seen in Renilla. Our videos show that light proceeds as waves along the colony from the point of stimulation for all three species, as observed in many other octocorals. Features of their bioluminescence are strongly suggestive of a "burglar alarm" function.

ecology↗

The genomic basis of animal origins: a chromosomal perspective from the sponge Ephydatia muelleri

The genomes of non-bilaterian metazoans are key to understanding the molecular basis of early animal evolution. However, a full comprehension of how animal-specific traits such as nervous systems arose is hindered by the scarcity and fragmented nature of genomes from key taxa, such as Porifera. Ephydatia muelleri is a freshwater sponge found across the northern hemisphere. Here we present its 326 Mb genome, assembled to high contiguity (N50: 9.88 Mb) with 23 chromosomes on 24 scaffolds. Our analyses reveal a metazoan-typical genome architecture, with highly shared synteny across Metazoa, and suggest that adaptation to the extreme temperatures and conditions found in freshwater often involves gene duplication. The pancontinental distribution and ready laboratory culture of E. muelleri make this a highly practical model system, which with RNAseq, DNA methylation and bacterial amplicon data spanning its development and range allows exploration of genomic changes both within sponges and in early animal evolution.

evolutionary biology↗

Profiling cellular diversity in sponges informs animal cell type and nervous system evolution

The evolutionary origin of metazoan cell types such as neurons, muscles, digestive, and immune cells, remains unsolved. Using whole-body single-cell RNA sequencing in a sponge, an animal without nervous system and musculature, we identify 18 distinct cell types comprising four major families. This includes nitric-oxide sensitive contractile cells, digestive cells active in macropinocytosis, and a family of amoeboid-neuroid cells involved in innate immunity. We uncover presynaptic genes in an amoeboid-neuroid cell type, and postsynaptic genes in digestive choanocytes, suggesting asymmetric and targeted communication. Corroborating this, long neurite-like extensions from neuroid cells directly contact and enwrap choanocyte microvillar collars. Our data indicate a link between neuroid and immune functions in sponges, and suggest that a primordial neuro-immune system cleared intruders and controlled ciliary beating for feeding.

developmental biology↗

A Hybrid de novo Assembly of the Sea Pansy (Renilla muelleri) Genome

BackgroundOver 3,000 species of octocorals (Cnidaria, Anthozoa) inhabit an expansive range of environments, from shallow tropical seas to the deep-ocean floor. They are important foundation species that create coral \"forests\" which provide unique niches and three-dimensional living space for other organisms. The octocoral genus Renilla inhabits sandy, continental shelves in the subtropical and tropical Atlantic and eastern Pacific Oceans. Renilla is especially interesting because it produces secondary metabolites for defense, exhibits bioluminescence, and produces a luciferase that is widely used in dual-reporter assays in molecular biology. Although several cnidarian genomes are currently available, the majority are from hexacorals. Here, we present a de novo assembly of the R. muelleri genome, making this the first complete draft genome from an octocoral.\n\nFindingsWe generated a hybrid de novo assembly using the Maryland Super-Read Celera Assembler v.3.2.6 (MaSuRCA). The final assembly included 4,825 scaffolds and a haploid genome size of 172 Mb. A BUSCO assessment found 88% of metazoan orthologs present in the genome. An Augustus ab initio gene prediction found 23,660 genes, of which 66% (15,635) had detectable similarity to annotated genes from the starlet sea anemone, Nematostella vectensis, or to the Uniprot database. Although the R. muelleri genome is smaller (172 Mb) than other publicly available, hexacoral genomes (256-448 Mb), the R. muelleri genome is similar to the hexacoral genomes in terms of the number of complete metazoan BUSCOs and predicted gene models.\n\nConclusionsThe R. muelleri hybrid genome provides a novel resource for researchers to investigate the evolution of genes and gene families within Octocorallia and more widely across Anthozoa. It will be a key resource for future comparative genomics with other corals and for understanding the genomic basis of coral diversity.

genomics↗

Very few sites can reshape a phylogenetic tree

The history of animal evolution, and the relative placement of extant animal phyla in this history is, in principle, testable from phylogenies derived from molecular sequence data. Though datasets have increased in size and quality in the past years, the contribution of individual genes (and ultimately amino acid sites) to the final phylogeny is unequal across genes. Here we demonstrate that by removing a small fraction of sites that strongly favor one topology, it is possible produce a highly-supported tree of an alternate topology. We explore this approach using a dataset for animal phylogeny, and create a highly-supported tree with a monophyletic group of sponges and ctenophores, a topology not usually recovered. As nearly all gene sets are neither standardized nor representative of the entire genome, we conclude that there are only two possible ways to remedy this problem. One solution would need to use a fixed set of genes, which though not representative, is at least standardized. The other would be to construct phylogenies using all genes, thus limiting analysis to species with sequenced genomes.

evolutionary biology↗

The role of homology and orthology in the phylogenomic analysis of metazoan gene content

Resolving animal (Metazoa) relationships is crucial to our understanding of, for example, the origin of their key traits such as muscles, guts and nerves. However, a broadly accepted metazoan consensus phylogeny has yet to emerge. In part this is because the genomes of deeply-diverging and fast-evolving lineages may undergo significant gene turnover, reducing the number of orthologs shared with related phyla. This can limit the usefulness of traditional phylogenetic methods that rely on alignments of orthologous sequences. Phylogenetic analysis of gene content has the potential to circumvent this orthology requirement, with binary presence/absence of homologous gene families representing a source of phylogenetically informative characters. Applying binary substitution models to the gene content of 26 complete animal genomes, we demonstrate that patterns of gene conservation differ markedly depending on whether gene families are defined by orthology or homology, i.e., whether paralogs are excluded or included. We conclude that the placement of deeply-diverging lineages, like ctenophores, may exceed the limit of resolution afforded by methods based on comparisons of orthologous protein supermatrices, and novel approaches are required to fully capture the evolutionary signal from genes within genomes.

evolutionary biology↗

The Genome Of The Contractile Demosponge Tethya wilhelma And The Evolution Of Metazoan Neural Signalling Pathways

Porifera are a diverse animal phylum with species performing important ecological roles in aquatic ecosystems, and have become models for multicellularity and early-animal evolution. Demosponges form the largest class in sponges, but previous studies have relied on the only draft demosponge genome of Amphimedon queenslandica. Here we present the 125-megabase draft genome of a contractile laboratory demosponge Tethya wilhelma, sequenced to almost 150x coverage. We explore the genetic repertoire of transporters, receptors, and neurotransmitter metabolism across early-branching metazoans in the context of the evolution of these gene families. Presence of many genes is highly variable across animal groups, with many gene family expansions and losses. Three sponge classes show lineage-specific expansions of GABA-B receptors, far exceeding the gene number in vertebrates, while ctenophores appear to have secondarily lost most genes in the GABA pathway. Both GABA and glutamate receptors show lineage-specific domain rearrangements, making it difficult to trace the evolution of these gene families. Gene sets in the examined taxa suggest that nervous systems evolved independently at least twice and either changed function or were lost in sponges. Changes in gene content are consistent with the view that ctenophores and sponges are the earliest-branching metazoan lineages and provide additional support for the proposed clade of Placozoa/Cnidaria/Bilateria.

genomics↗