Diet-induced shifts in the crown-of-thorns (Acanthaster sp.) larval microbiome

Carrier, Tyler J.; Wolfe, Kennedy; López, Karen; Gall, Mailie; Janies, Daniel; Byrne, Maria; Reitzel, Adam M.

doi:10.1007/s00227-018-3416-x

Cited by 32 publications

(30 citation statements)

References 49 publications

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“…Second, clonal larvae of the sea star Luidia collected from the Gulf Stream had one to three rodshaped morphotypes of subcuticle bacteria (Bosch, 1992). For Luidia as well as Acanthaster, some symbionts were located in the gut and auto-fluoresced (Bosch, 1992;Galac et al, 2016;Carrier et al, 2018b), suggesting the potential ability to be phototrophic. Collectively, these examples suggest, but do not show explicitly, that bacterial symbionts may have metabolic functions that could potentially benefit the larval host.…”

Section: Subcuticle Bacteriamentioning

confidence: 99%

Symbiotic Life of Echinoderm Larvae

Carrier

Reitzel

2020

Front. Ecol. Evol.

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Echinoderm larvae have served as a fundamental system for understanding development and life history evolution over much of the last century. In the last few decades, our understanding of echinoderm larvae has expanded to the microbiota that they associate with. These symbionts and the communities that they form in relation to echinoderm larval host are the focus of this review. Our synthesis of the literature suggests three primary themes. First, larval echinoderms associate with "subcuticle bacteria" that appear to colonize select tissue types. Second, the bacterial communities associated with larval echinoderms exhibit compositional shifts that are correlated with several fundamental properties of larval biology (e.g., development and morphological plasticity) and ecology (e.g., feeding environment). Third, echinoderm larvae exhibit specific responses to pathogenic bacteria that may aid in maintaining the symbiont community and avoid dysbiosis. To our knowledge, no studies have focused on whether climate-related stressors impact the composition of these symbiont communities or how changes in bacteria may modulate response by larvae to these environmental stressors. Lastly, we conclude by outlining techniques that need to be established in echinoderm larvae to transition from correlations between larvae and their associated microbiota to the function of these symbionts.

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Section: Subcuticle Bacteriamentioning

confidence: 99%

Symbiotic Life of Echinoderm Larvae

Carrier

Reitzel

2020

Front. Ecol. Evol.

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“…The laboratory and natural microbiomes have several qualitative similarities: both are predominantly Alphaproteobacteria and Gammaproteobacteria, with minimal diversity at zygote stage and increasing diversity over time (significant in NSW, not in AEW; Figure 3; Supplementary Figures 3, 5, 6, Supplementary Table 1). Additionally, larvae in both environments were hosts to bacterial communities significantly different from the surrounding seawater and from their Rhodomonas feeding cultures, suggesting a degree of selective colonization (Supplementary Figure 4) (28,29,31). This effect may be related to the increased alkalinity of the larval gut relative to their environment (80), as bacteria able to thrive in such environments could be positively selected.…”

Section: Larval 16s Sequence Diversity In the Laboratory And Natural mentioning

confidence: 99%

“…Associated bacteria have been characterized in diverse echinoderm taxa at many stages of development (22,(26)(27)(28)(29)(30)(31), but spatiotemporal colonization kinetics in sea urchin larva remain poorly described (19,69). Two likely sites for bacterial colonization are the larval digestive tract and the ectoderm, whether its external surface or the subcuticular space (70,71).…”

Section: Kinetics Of Bacterial Colonizationmentioning

confidence: 99%

“…Ilya Metchnikoff first described cellular immunity in echinoderm larvae in the late 1800s (20), and recently, researchers have returned to these organisms with modern genomic, experimental, and imaging techniques, describing the specialized immune cell types of echinoderm larvae and their functions in response to diverse challenges [e.g., (21)(22)(23)(24); reviewed in (17,19,25)]. In parallel, embryonic, larval, and adult echinoderm bacterial microbiomes have been characterized in several species [e.g., (22,(26)(27)(28)(29)(30)(31); reviewed in (19)]. These studies focused on bacteria acquired in natural seawater or in the wild, but major questions that remain are to what degree artificial seawater-raised laboratory animals recapitulate the microbiota of their wild counterparts (32,33) and how these differences Abbreviations: FSW, artificial filtered seawater; P/S, 0.2 µm-filtered artificial seawater + 100 U/mL penicillin, 100 µg/mL streptomycin; AEW, artificial filtered seawater + 20% (v/v) adult-exposed tank water; CFU, colony-forming unit; dpf, days post fertilization; NSW, natural seawater; hpf, hours post fertilization; OTU, operational taxonomic unit; PCoA, principle coordinate analysis.…”

Section: Introductionmentioning

confidence: 99%

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Bacterial Exposure Mediates Developmental Plasticity and Resistance to Lethal Vibrio lentus Infection in Purple Sea Urchin (Strongylocentrotus purpuratus) Larvae

et al. 2020

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Exposure to and colonization by bacteria during development have wide-ranging beneficial effects on animal biology but can also inhibit growth or cause disease. The immune system is the prime mediator of these microbial interactions and is itself shaped by them. Studies using diverse animal taxa have begun to elucidate the mechanisms underlying the acquisition and transmission of bacterial symbionts and their interactions with developing immune systems. Moreover, the contexts of these associations are often confounded by stark differences between "wild type" microbiota and the bacterial communities associated with animals raised in conventional or germ-free laboratories. In this study, we investigate the spatio-temporal kinetics of bacterial colonization and associated effects on growth and immune function in larvae of the purple sea urchin (Strongylocentrotus purpuratus) as a model for host-microbe interactions and immune system development. We also compare the host-associated microbiota of developing embryos and larvae raised in natural seawater or exposed to adult-associated bacteria in the laboratory. Bacteria associated with zygotes, embryos, and early larvae are detectable with 16S amplicon sequencing, but 16S-FISH indicates that the vast majority of larval bacterial load is acquired after feeding begins and is localized to the gut lumen. The bacterial communities of laboratory-cultured embryos are significantly less diverse than the natural microbiota but recapitulate its major components (Alphaproteobacteria, Gammaproteobacteria, and Bacteroidetes), suggesting that biologically relevant host-microbe interactions can be studied in the laboratory. We also demonstrate that bacterial exposure in early development induces changes in morphology and in the immune system. In the absence of bacteria, larvae grow larger at the 4-arm stage. Additionally, Schuh et al.Bacteria-Mediated Developmental Plasticity bacteria-exposed larvae are significantly more resistant to lethal infection with the larva-associated pathogen Vibrio lentus suggesting that early exposure to high levels of microbes, as would be expected in natural conditions, affects the immune state in later larvae. These results expand our knowledge of microbial influences on early sea urchin development and establish a model in which to study the interactions between the developing larval immune system and the acquisition of larval microbiota.

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“…Despite their potential biological importance, studies of the bacteria associated with COTS have been mostly culture-based, and only two culture-independent studies have been published to date. Carrier et al reported shifts in COTS larval microbiomes with diet [20]. Høj et al found that adult COTS have tissue-specific bacterial communities, largely comprising four major bacterial groups: Mollicutes in male gonads, Spirochaetales in the body wall, Hyphomonadaxeae in the tube feet, and Oceanospirillales in all tissues [21].…”

Section: Introductionmentioning

confidence: 99%

A universal subcuticular bacterial symbiont of a coral predator, the crown-of-thorns starfish, in the Indo-Pacific

Wada

Yuasa

Kajitani

et al. 2020

Preprint

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Background:Population outbreaks of the crown-of-thorns starfish (Acanthaster planci sensu lato；COTS), a primary predator of reef-building corals in the Indo-Pacific Ocean, are major concernｓ in coral reefs management. While biological and ecological knowledge on COTS has been accumulated since the 1960s, little is known about their associated bacteria. The aim of this study was to provide fundamental information on dominant COTS-associated bacteria by multidisciplinary approach. Methods:We first conducted 16S rRNA metabarcoding for bacterial profiles on different body parts of COTS, and obtained full-length 16S rRNA gene sequence of the single dominant bacterium for phylogenetic analysis. A total 205 COTS individuals from 17 locations throughout the Indo-Pacific Ocean was examined for the presence of COTS associated bacteria (named COTS27). The COTS27 localization was visualized by Fluorescence in situ hybridization (FISH) using a COTS27-specific probe. Furthermore, COTS27 chromosome genome was reconstructed from the hologenome sequence data of COTS. Results:We discovered that a single bacterium exists at high densities in the subcuticular space of COTS forming a biofilm-like structure over the entire body surface of COTS. COTS27 belongs to a clade that presumably represents a distinct order (so-called marine spirochetes) in the phylum Spirochaetes and is universally present in COTS throughout the Indo-Pacific Ocean. The reconstructed genome of COT27 includes some genetic traits that are probably linked to adaptation to marine environments and evolution as an extracellular endosymbiont in subcuticular spaces. Conclusions:COTS27 can be found in the allopatrically spectated 3 different COTS species, ranging from northern Red Sea to the central Pacific, implying symbiotic relationship started before speciation (about 2 million years ago). The universal and nearly mono-specific association of COTS27 with COTS potentially provides a useful model system to study symbiont-host interactions in marine invertebrates.3

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Diet-induced shifts in the crown-of-thorns (Acanthaster sp.) larval microbiome

Cited by 32 publications

References 49 publications

Symbiotic Life of Echinoderm Larvae

Symbiotic Life of Echinoderm Larvae

Bacterial Exposure Mediates Developmental Plasticity and Resistance to Lethal Vibrio lentus Infection in Purple Sea Urchin (Strongylocentrotus purpuratus) Larvae

A universal subcuticular bacterial symbiont of a coral predator, the crown-of-thorns starfish, in the Indo-Pacific

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