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Biology subjects

Hadfield, M. G.

Publications and source records attributed to Hadfield, M. G..

10 recordsLinked to original sources

Complex benthic habitats retain larvae sinking in response to soluble cues: field study of coral reefs in wave-driven flow

Many benthic marine invertebrates disperse by releasing microscopic larvae carried by ocean currents to new sites, where they must settle into appropriate habitats and metamorphose to recruit. Species whose larvae settle in response to water-borne chemical cues live in topographically complex habitats. To study whether sinking in response to dissolved cues affects retention of larvae within complex habitats exposed to ambient water flow moving faster than larvae sink, we used the reef-dwelling sea slug, Phestilla sibogae, whose competent larvae stop swimming and sink in response to dissolved cue from their prey coral, Porites compressa. We conducted field experiments where dye-labelled water, neutrally buoyant particles, and larval mimics (particles that sank at the velocity of larvae of P. sibogae) were released together upstream of reefs of branching corals to determine if larval sinking in water above and within a reef affects larval retention within the reef. Wave-driven water flow measured above a reef in the field had instantaneous velocities peaking at 0.3 m s-1, driving slow net advection of water shoreward at [~]0.02 m s-1. Much slower wave-driven flow moved through the interstices within the reef. In this field flow, sinking by larval mimics caused their retention within a reef after dye-labelled water and neutrally buoyant particles had left. Such retention of sinking larvae within topographically complex benthic communities enhances successful recruitment by exposing larvae to high concentrations of cue for long periods, allowing them time to sink to surfaces, adhere, and undergo metamorphosis.

ecology↗

Biodegradable Plastics in the Marine Environment: Comparative Analyses of Bacterial Biofilms, Macroinvertebrate Colonization, and Degradation Patterns

Floating debris in the ocean recruits microbes and marine invertebrates to its surface, resulting in rafting communities. As biodegradable plastics increase in prevalence as alternatives to petroleum-based plastics, their properties may impact the dynamics of rafting communities by influencing the composition of bacterial biofilms and attached invertebrates. We compared attached biofouling communities of bacteria and marine invertebrates on biodegradable surfaces and nonbiodegradable petroleum-based plastics and naturally occurring substrata. Six surface types: polypropylene plastic (PP), polystyrene (PS), polylactic acid plastic (PLA), polyhydroxyalkanoates plastic (PHA), maple wood veneer, and propagules of the mangrove Rhizophora mangle, were examined to determine if plastic type affected biofilm composition on the surfaces and their degradation patterns. Biofilm analyses were conducted at twelve weeks, and degradation analyses were conducted at twenty-two weeks of immersion. Using digital image analysis, 16S rRNA sequencing, and metagenomic analyses, we found that microbial biofilms, marine invertebrate inhabitants, and degradation patterns differed across the various substrate types tested. Microbial communities on PLA were more similar to those on the two non-biodegradable plastics, while communities on PLA were more like those on the natural substrata. The biodegradable PLA showed signs of degradation within 22 weeks of immersion, suggesting that biodegradable plastics behave variably in the natural environment. Results of this study bring forth the importance of designing biodegradable plastics with careful consideration of the environmental conditions in which they are likely to persist.

ecology↗

Strain-Specific Surface Polysaccharides Mediate BacterialInduction of Metamorphosis in the coralPocillopora acuta

Coral-reef ecosystem persistence depends on successful larval recruitment, a process increasingly jeopardized by climate change and other anthropogenic stressors. Microbial biofilms induce larval settlement and metamorphosis in marine invertebrates, including corals, but specific molecular cues for corals remain unclear. Glycosylated lipids and polysaccharides from crustose coralline algae (CCA), along with bacterial small molecules, are proposed inducers, but their effects vary by coral species, bacterial strain, and environment, highlighting the need to clarify their molecular basis and specificity. Here, we identify bacterial lipopolysaccharide (LPS), specifically its O-antigen polysaccharide component, as a potent settlement cue for larvae of the coral Pocillopora acuta. Using purified LPS from diverse marine bacteria, we show that inductive activity is bacterial species and strain specific and correlates with the structure of O-antigen. These findings support a glycan-centred mechanism of coral recruitment, implicating microbial surface chemistry as a key determinant of larval settlement. By demonstrating a specific and functional role for O-antigen, we expand the ecological relevance of bacterial glycans beyond immunity and pathogenesis, highlighting their role in key developmental and ecological transitions in marine invertebrates. As coral reefs face escalating environmental pressures, employing such signals offers a promising strategy to enhance larval settlement and support reef restoration.

ecology↗

Evolutionary history of the widespread association between placozoans and diverse Rickettsiales symbionts

Rickettsiales are an enigmatic clade of strictly host-associated bacteria with some very common phylotypes in aquatic habitats. Despite amplicon- and metagenomic sequencing-based observations, the roles of these aquatic Rickettsiales are still unknown, as their genomes feature both beneficial and parasitic traits. In placozoans, microscopy-based observations of intracellular and Rickettsia-like-organisms point to Rickettsiales as common and abundant symbionts. We therefore systematically studied the microbiomes of placozoans to understand the eco-evolutionary dynamics of their associated Rickettsiales. Single-animal metagenomics revealed a widespread association of placozoans with Rickettsiales from three clades of Ca. Midichloriaceae, which were present in all but two placozoan lineages. A comparative phylogenetic analysis of placozoans and their Rickettsiales symbionts revealed host species-specific switches among Rickettsiales clades in several placozoan lineages. Our combination of evolutionary analyses, genome annotations, and expression data indicate different functional roles of these Rickettsiales clades, with some clearly diverging from a classical parasitic lifestyle by the loss of all ATP scavenging machinery. One of placozoan lineages that lacked Ca. Midichloriaceae was instead associated with Rickettsiaceae symbionts, while another was completely devoid of Rickettsiales symbionts. Our imaging data of fibre cells entirely free of Rickettsiales underscores previously unrecognized variation in placozoan-microbe associations. Early-branching invertebrates, including placozoans as well as many corals, are gaining increasing traction as emerging models across the life sciences. Our data and analyses show that it is important to consider the specific endosymbiont groups and their ecology in a given host, as these symbionts likely influence the hosts cellular and organismal biology.

microbiology↗

Bacteria-powered living materials enable coral larval settlement

The global decline of coral reefs calls for new strategies to rapidly restock coral populations and maintain ecosystem functions and services. Low recruitment success on degraded reefs hampers coral sexual propagation and contributes to limited genetic diversity and reef resilience. Here, we introduce a living bacteria-powered reef ink (Brink) for assisted coral recruitment. Brink can be rapidly applied to restoration substrates via photopolymerization, and it has been formulated to cultivate two settlement-inducing bacterial strains (Cellulophaga lytica and Thalassotalea euphylliae). Settlement assays performed with broadcast spawning (Montipora capitata) and brooding (Pocillopora acuta) Indo-Pacific corals showed that Brink-coated substrates increased settlement >5-fold compared to uncoated control substrates. Brink can be applied as a coating or 3D bioprinted, leading to various potential applications for integration with reef engineering. Our approach underscores the potential of using functional living materials for augmented ecosystem engineering and reef rehabilitation. SynopsisThis study introduces a functional and sustainable bacteria-powered living material that enhances coral settlement, promoting coral reef rehabilitation and ecosystem resilience.

bioengineering↗

The natural sequence of events in larval settlement and metamorphosis of Hydroides elegans (Polychaeta; Serpulidae)

The broadly distributed serpulid worm Hydroides elegans has become a model organism for studies of marine biofouling, development and the processes of larval settlement and metamorphosis induced by surface microbial films. Contrasting descriptions of the initial events of these recruitment processes, whether settlement is induced by (1) natural multi-species biofilms, (2) biofilms composed of single bacterial species known to induce settlement, or (3) a bacterial extract stimulated the research described here. We found that settlement induced by natural biofilms or biofilms formed by the bacterium Pseudoalteromonas luteoviolacea is invariably initiated by attachment and secretion of an adherent and larva-enveloping primary tube, followed by loss of motile cilia and ciliated cells and morphogenesis. The bacterial extract containing complex tailocin arrays derived from an assemblage of phage genes incorporated into the bacterial genome appears to induce settlement events by destruction of larval cilia and ciliated cells, followed by attachment and primary-tube formation. Similar destruction occurred when precompetent larvae and larvae of a nudibranch gastropod were exposed to the extract, neither of which metamorphosed. We further argue that larvae that lose their cilia before attachment would be swept away from the sites that stimulated settlement by the turbulent flow characteristic of most marine habitats.

developmental biology↗

Laser ablation of the apical sensory organ of Hydroides elegans does not inhibit detection of metamorphic cues

Larvae of many marine invertebrates bear an anteriorly positioned apical sensory organ (ASO) presumed to be the receptor for settlement- and metamorphosis-inducing environmental cues, based on its structure, position and observed larval behavior. Larvae of the polychaete Hydroides elegans are induced to settle by bacterial biofilms, which they explore with their ASO and surrounding anteroventral surfaces. A micro-laser was utilized to destroy the ASO and other anterior ciliary structures in competent larvae of H. elegans. After ablation, larvae were challenged with bacterial biofilmed or clean surfaces and percent metamorphosis was determined. Ablated larvae were also assessed for cellular damage by applying fluorescently tagged FMRF-amide antibodies and observing the larvae by laser-scanning confocal microscopy. While the laser pulses caused extensive damage to the ASO and surrounding cells, they did not inhibit metamorphosis. We conclude that the ASO is not a required receptor site for cues that induce metamorphosis. Summary StatementLarvae of the polychaete Hydroides elegans retain the capacity to sense biofilm cues and metamorphose despite removal of their apical sensory organs, the supposed sensors for settlement cues.

zoology↗

Bacterial lipopolysaccharide induces settlement and metamorphosis in a marine larva

How larvae of the many phyla of marine invertebrates find places appropriate for settlement, metamorphosis, growth and reproduction is an enduring question in marine science. Biofilm induced metamorphosis has been observed in marine invertebrate larvae from nearly every major marine phylum. Despite the widespread nature of this phenomenon the mechanism of induction remains poorly understood. The serpulid polychaete Hydroides elegans is a well-established model for investigating bacteria-induced larval development. A broad range of biofilm bacterial species elicit larval metamorphosis in H. elegans via at least two mechanisms, including outer membrane vesicles and phage-tail bacteriocins. We investigated the interaction between larvae of H. elegans and the inductive bacterium Cellulophaga lytica, which produces an abundance of OMVs but not phage-tail bacteriocins. We asked whether the OMVs of C. lytica induce larval settlement due to cell membrane components or through delivery of specific cargo. Employing a biochemical structure-function approach with a strong ecological focus, the cells and outer membrane vesicles produced by C. lytica were interrogated to determine the nature of the inductive molecule. Here we report that the cue produced by C. lytica that induces larvae of H. elegans to metamorphose is lipopolysaccharide (LPS). The widespread prevalence of LPS and its associated taxonomic and structural variability suggest it may be a broadly employed cue for bacterially induced larval settlement of marine invertebrates. Significance StatementNew surfaces in the sea are quickly populated by dense communities of invertebrate animals, whose establishment and maintenance require site-specific settlement of larvae from the plankton. Although it is recognized that larvae selectively settle in sites where they can metamorphose and thrive, and that the biofilm bacteria residing on these surfaces supply inductive cues, the nature of the cues used to identify right places has remained enigmatic. In this paper, we reveal that lipopolysaccharide (LPS) from the outer membrane of a marine Gram-negative bacterium cue metamorphosis for a marine worm and discuss the likelihood that LPS provides the variation necessary to explain settlement site selectivity for many of the bottom-living invertebrate animals that metamorphose in response to bacterial biofilms.

ecology↗

The Trichoplax microbiome: the simplest animal lives in an intimate symbiosis with two intracellular bacteria

Summary paragraphPlacozoa is an enigmatic phylum of simple, microscopic, marine metazoans. Although intracellular bacteria have been found in all members of this phylum, almost nothing is known about their identity, location and interactions with their host. We used metagenomic and metatranscriptomic sequencing of single host individuals, plus metaproteomic and imaging analyses, to show that the placozoan Trichoplax H2 lives in symbiosis with two intracellular bacteria. One symbiont forms a new genus in the Midichloriaceae (Rickettsiales) and has a genomic repertoire similar to that of rickettsial parasites, but does not appear to express key genes for energy parasitism. Correlative microscopy and 3-D electron tomography revealed that this symbiont resides in an unusual location, the rough endoplasmic reticulum of its hosts internal fiber cells. The second symbiont belongs to the Margulisbacteria, a phylum without cultured representatives and not known to form intracellular associations. This symbiont lives in the ventral epithelial cells of Trichoplax, likely metabolizes algal lipids digested by its host, and has the capacity to supplement the placozoans nutrition. Our study shows that even the simplest animals known have evolved highly specific and intimate associations with symbiotic, intracellular bacteria, and highlights that symbioses with microorganisms are a basal trait of animal life.

microbiology↗

Placozoans are eumetazoans related to Cnidaria

The phylogenetic placement of the morphologically simple placozoans is crucial to understanding the evolution of complex animal traits. Here, we examine the influence of adding new genomes from placozoans to a large dataset designed to study the deepest splits in the animal phylogeny. Using site-heterogeneous substitution models, we show that it is possible to obtain strong support, in both amino acid and reduced-alphabet matrices, for either a sister-group relationship between Cnidaria and Placozoa, or for Cnidaria and Bilateria (=Planulozoa), also seen in most published work to date, depending on the orthologues selected to construct the matrix. We demonstrate that a majority of genes show evidence of compositional heterogeneity, and that the support for Planulozoa can be assigned to this source of systematic error. In interpreting this placozoan-cnidarian clade, we caution against a peremptory reading of placozoans as secondarily reduced forms of little relevance to broader discussions of early animal evolution.

zoology↗