Biology subjects

Nichols, S. A.

Publications and source records attributed to Nichols, S. A..

9 recordsLinked to original sources

bioRxiv2026

The discovery of an external bacterial niche reconciles sequencing-based microbiomes in a freshwater sponge

Animals maintain beneficial associations with microbes while avoiding parasitism, often by physically segregating microbes from host tissues. However, sponges (Porifera) are frequently cited as an exception, with bacteria being shown to reside directly within the host mesohyl--an interior space composed of extracellular matrix and migratory cells. Yet this model rests largely on studies of field-collected specimens, where experimental control and spatial resolution are limited. Here, we exploit the experimental advantages of the freshwater sponge Ephydatia muelleri--culturable in the laboratory and highly amenable to confocal imaging--to directly address the spatial organization and transmission of host-associated bacteria. Contrary to expectations from studies of marine sponge systems, and to predictions from microbiome sequencing studies of freshwater sponges, we found limited evidence for diverse bacterial communities inhabiting the mesohyl of E. muelleri. Instead, we identified a novel microbial niche that is external to sponge tissues--a host-secreted matrix that underlies the basal epithelium, coats spicules, and envelops gemmules. In both laboratory cultures and field-collected specimens, matrix-associated microbes were abundant but separated from the sponge interior (mesohyl) by a continuous epithelial barrier. These external matrix-associated communities may contribute to the molecular signatures of stable freshwater sponge microbiomes, even if their functional roles remain unresolved. These findings reframe sequencing-based reports of freshwater sponge microbiomes with confocal imaging, and highlight that spatial context is essential for interpreting animal host-microbe associations. O_FIG O_LINKSMALLFIG WIDTH=175 HEIGHT=200 SRC="FIGDIR/small/704605v2_ufig1.gif" ALT="Figure 1"> View larger version (67K): org.highwire.dtl.DTLVardef@151ec39org.highwire.dtl.DTLVardef@16bca41org.highwire.dtl.DTLVardef@1ab807eorg.highwire.dtl.DTLVardef@80d83b_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOGraphical AbstractC_FLOATNO Microbial communities colonize the skeletal matrix during dormancy in E. muelleri. In contrast to interpretations from microbiome sequencing studies, we find limited evidence for a resident microbiome within the mesohyl (shown in green) of the freshwater sponge, Ephydatia muelleri. Instead, we find that microbes are primarily confined to a novel external nichea host-secreted matrix (shown in brown), which is exposed to the environment during periods of dormancy, and therefore permissive to microbial colonization. This matrix confers attachment to the basal substrate, embeds siliceous spicules, and coats gemmules (stress-resistant propagules maintaining senesced tissues). We find no evidence of bacteria being maintained across dormancy through the interior of gemmules. Instead, the external matrix and associated microbes are physically separated from the host mesohyl by a continuous epithelium (depicted as thick black lines). With spatial context afforded by in vivo imaging, we propose that these external-matrix-resident microbes likely account for previous reports of a stable, internal microbiome in freshwater sponges. C_FIG

ecology↗

bioRxiv2026

The fossil record of siliceous sponge spicules can be taken at face value

Modern sponges (Porifera) diverged by the Cryogenian, but their silicious skeletons do not appear in the fossil record until one hundred million years later, a time-span termed the "spicule gap" and thought to be a taphonomic artifact even though sponges convergently evolved siliceous spicules. Due to sponges position in animal phylogeny and important role in regulating ocean chemistry, the timing of their biomineralization has major implications for the changing tempo and mode of Earth systems as animals radiate. In a comprehensive dataset of Ediacaran and Cambrian sponges, we find that spicules are readily preserved in Cambrian environments more extreme than those of the Ediacaran. Given the convergent evolution of siliceous spicules, we find that the fossil record accurately represents when spicules first evolved in the different sponge lineages.

paleontology↗

bioRxiv2026

Co-option of Lysosomal Machinery for Biomineralization

Biomineralization evolved repeatedly across animals, resulting in novel strategies for buoyancy, locomotion, and defense. Sponges are the only metazoans that build a silica-based skeleton and the mechanisms underlying their biosilicification are relatively understudied compared to other major silicifiers. Here, we show that in freshwater sponges, cells specialized for biosilicification, termed sclerocytes, highly express lysosomal-associated genes, including the V-H+-ATPase (VHA) proton pump, oculocutaneous albinism type 2 (OCA2) anion channels, cathepsins, silicateins, TMEM55A/B, TMEM192, TMEM199, and other proteins involved in lysosomal maintenance and degradation. We demonstrate that VHA protein localizes to the sclerocyte silica deposition vesicle (SDV) and that VHA-dependent SDV acidification is essential for silica spicule formation. This function mirrors the role of VHA in diatom biosilicification and in biocalcification across a broad sweep of taxa. We also found that genes homologous to the plant silicon efflux transporter Lsi2 are highly upregulated in sclerocytes and confirmed their localization using Hybridization Chain Reaction Fluorescence In Situ Hybridization (HCR-FISH). These results corroborate phylogenetic and transcriptomic evidence that Lsi2 homologs are involved in sponge silicic acid transport. Data mining of previous studies revealed many of the sponge sclerocyte lysosomal-associated genes have been correlated with biomineralization across eukaryotes, including coccolithophores, bryozoans, crustaceans, mollusks, and mammals. As detoxification was a likely driver for the evolution of biomineralization, we propose that lysosomal machinery aided in detoxification by allowing sponges to sequester Si in acidified compartments to prevent its catastrophic intracellular precipitation. This lysosomal toolkit was likely independently co-opted for the formation of biomineralized structures in multiple species.

cell biology↗

bioRxiv2025

Genomic connectivity and adaptation signals of the freshwater sponge Ephydatia muelleri across its distribution

1.Freshwater sponges fulfill critical ecological functions, including maintaining water quality, regulating nutrient dynamics, offering habitats for diverse taxa, and serving as a vital food source for various species. However, their patterns of dispersal and genetic connectivity remain inadequately understood, posing significant challenges to effective conservation assessments. We examined genetic connectivity and genetic adaptation to local environmental conditions in Ephydatia muelleri across its geographic range using ddRADseq-derived SNPs from 106 individuals collected from 11 localities spanning North America, Europe, and Asia. Analysis of 3,182 neutral SNPs revealed low connectivity and strong genetic structure among regions within two main genetic clusters of North America and Eurasia, while 115 SNPs identified to be under selection showed considerable evidence for differentiated, polygenic adaptation to light and temperature conditions across sampled locations, as well as selection on gene regulatory processes. These findings align with the "monopolization hypothesis", suggesting that historical climatic and geological conditions of the Last Glacial Maximum, including habitat expansion, contraction, and natural barriers, have contributed more to the current genetic structure of E. muelleri populations than contemporary gene flow, which is restricted by monopolistic habitat colonization by this species. Our results provide novel support for ecological theory on dispersal in aquatic invertebrates, as well as insights into the plasticity of E. muelleri in the face of varying environmental conditions that are fundamentally important for freshwater ecosystem conservation.

evolutionary biology↗

bioRxiv2024

Proteomic analysis of the Aggregation Factor from the sponge Clathria (Microciona) prolifera suggests an ancient protein domain toolkit for allorecognition in animals

The discovery that sponges (Porifera) can fully regenerate from aggregates of dissociated cells launched them as one of the earliest experimental models for cell adhesion and allorecognition studies in animals. This process depends on an extracellular glycoprotein complex called the Aggregation Factor (AF). However, our understanding of how animal adhesion and allorecognition mechanisms first evolved is complicated by the fact that the known components of the AF are thought to be unique to sponges. We used label-free quantitative proteomics to identify additional AF components and interacting proteins in the classical model Clathria prolifera and compare them to proteins involved in cell interactions in Bilateria. Our results confirm MAFp3/p4 as the primary components of the AF, but implicate related proteins with calx-beta and wreath domains as additional components. Using AlphaFold, we unveiled close structural similarities of AF components to distant homologs in other animals, previously masked by the stark decay of sequence similarity. The wreath domain, believed to be unique to the AF, was predicted to contain a central beta-sandwich of the same organization as the vWFD domain in extracellular, gel-forming gly-coproteins in other animals. Additionally, we co-purified candidate AF-interacting proteins that share a conserved C-terminus, containing divergent Ig-like and Fn3 domains, a combination also known from IgCAMs. One of these, MAFAP1, may function to link the AF to the surface of cells. Our results highlight the existence of an ancient toolkit of conserved protein domains regulating cell-cell and cell-ECM interactions in all animals, and likely reflect a common origin of cell-adhesion and allorecognition.

biochemistry↗

bioRxiv2021

A muscle-related contractile tissue specified by MRTF-activity in Porifera

Muscle-based movement is a hallmark of animal biology, but the evolutionary origins of myocytes - the cells that comprise muscle tissues - are unknown. Sponges (Porifera) provide an opportunity to reconstruct the earliest periods of myocyte evolution. Although sponges are believed to lack muscle, they are capable of coordinated whole-body contractions that purge debris from internal water canals. This behavior has been observed for decades, but their contractile tissues remain uncharacterized; it is an open question whether they have affinity to muscle or non-muscle contractile tissues in other animals. Here, we characterize the endothelial-like lining of water canals (the endopinacoderm) as a primary contractile tissue in the sponge Ephydatia muelleri. We find tissue-wide organization of contractile actin-bundles that contain striated-muscle myosin II and transgelin, and that contractions are regulated by the release of internal Ca2+ stores upstream of the myosin-light-chain-kinase (MLCK) pathway. Further, we show that the endopinacoderm is developmentally specified by myocardin-related transcription factor (MRTF) as part of an environmentally-inducible transcriptional complex that otherwise is known to function in muscle development, plasticity, and regeneration in other animals. We conclude that both muscle tissues and the endopinacoderm evolved from a common, multifunctional contractile tissue in the animal stem-lineage. Furthermore, as an actin-regulated force-sensor, MRTF-activity offers a mechanism for how water canals dynamically remodel in response to flow and can re-form normally from stem-cells in the absence of the intrinsic positional cues characteristic of embryogenesis in other animals.

evolutionary biology↗

bioRxiv2019

Diverse cell junctions with unique molecular composition in tissues of a sponge (Porifera)

The integrity and organization of animal tissues depends upon specialized protein complexes that mediate adhesion between cells with each other (cadherin-based adherens junctions), and with the extracellular matrix (integrin-based focal adhesions). Reconstructing how and when these cell junctions evolved is central to understanding early tissue evolution in animals. We examined focal adhesion protein homologs in tissues of the freshwater sponge, Ephydatia muelleri (phylum Porifera). We found that sponge homologs of focal adhesion proteins co-precipitate as a complex and localize to cell junctions in sponge tissues. These data support that the adhesion roles of these proteins evolved early, prior to the divergence of sponges and other animals. However, in contrast to the spatially partitioned distribution of cell junctions in epithelia of other animals, focal adhesion proteins were found to be co-distributed with the adherens junction protein Em{beta}-catenin in sponge tissues; both at certain cell-cell and cell-extracellular matrix (ECM) adhesions. Sponge adhesion structures were found to be unique in other ways, too. The basopinacoderm (substrate-attachment epithelium) lacks typical polarity in that cell-ECM adhesions form on both basal and apical surfaces, and compositionally unique cell junctions form at the interface between cells with spicules (siliceous skeletal elements) and between cells and environmental bacteria. These results clarify the diversity, distribution and molecular composition of cell junctions in tissues of E. muelleri, but raise new questions about their function and homology with cell junctions in other animals.

evolutionary biology↗

bioRxiv2017

β-catenin has both conserved and novel functions in the sponge Ephydatia muelleri

{beta}-catenin acts as a transcriptional co-activator in the Wnt/{beta}-catenin signaling pathway and a cytoplasmic effector in cadherin-based cell adhesion. These functions are ancient within animals, but the earliest steps in {beta}-catenin evolution remain unresolved due to limited data from key lineages - sponges, ctenophores and placozoans. Previous studies in sponges have characterized {beta}-catenin expression dynamics and used GSK3B antagonists to ectopically activate the Wnt/{beta}-catenin pathway; both approaches rely upon untested assumptions about the conservation of {beta}-catenin function and regulation in sponges. Here, we test these assumptions using an antibody raised against {beta}-catenin from the sponge Ephydatia muelleri. We find that cadherin-complex genes co-precipitate with endogenous Em {beta}-catenin from cell lysates, but that Wnt pathway components do not. However, through immunostaining we detect both cell boundary and nuclear populations, and we find evidence that Em {beta}-catenin is a conserved substrate of GSK3B. Collectively, these data support conserved roles for Em {beta}-catenin in both cell adhesion and Wnt signaling. Additionally, we find evidence for an Em {beta}-catenin population associated with the distal ends of F-actin stress fibers in apparent cell-substrate adhesion structures that resemble focal adhesions. This finding suggests a fundamental difference in the adhesion properties of sponge tissues relative to other animals, in which the adhesion functions of {beta}-catenin are typically restricted to cell-cell adhesions.

evolutionary biology↗

bioRxiv2017

Transcriptome sequencing and delimitation of cryptic Oscarella species (O. carmela and O. pearsei sp. nov) from California, USA.

The homoscleromorph sponge Oscarella carmela, first described from central California, USA is shown to represent two morphologically similar but phylogenetically distant species that are co-distributed. We here describe a new species as Oscarella pearsei, sp. nov. and redescribe Oscarella carmela; the original description was based upon material from both species. Further, we correct the identification of published genomic/transcriptomic resources that were originally attributed to O. carmela, and present new Illumina-sequenced transcriptome assemblies for each of these species, and the mitochondrial genome sequence for O. pearsei sp. nov. Using SSU and LSU ribosomal DNA and the mitochondrial genome, we report the phylogenetic relationships of these species relative to other Oscarella species, and find strong support for placement of O. pearsei sp. nov. in a clade defined by the presence of spherulous cells that contain paracrystalline inclusions; O. carmela lacks this cell type and is most closely related to the Western Pacific species, O. malakhovi. Oscarella pearsei sp. nov and O. carmela can be tentatively distinguished based upon gross morphological differences such as color, surface texture and extent of mucus production, but can be more reliably identified using mitochondrial and nuclear barcode sequencing, ultrastructural characteristics of cells in the mesohyl, and the morphology of the follicle epithelium which surrounds the developing embryo in reproductively active individuals. Usually, cryptic species are very closely related to each other, but in this case and in sponges generally, cryptic species may be very distantly related because sponges can be difficult to identify based upon gross morphological characteristics.

evolutionary biology↗