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Acid secretion by the boring organ of the burrowing giant clam, Tridacna crocea.

ABSTRACT: The giant clam Tridacna crocea, native to Indo-Pacific coral reefs, is noted for its unique ability to bore fully into coral rock and is a major agent of reef bioerosion. However, T. crocea's mechanism of boring has remained a mystery despite decades of research. By exploiting a new, two-dimensional pH-sensing technology and manipulating clams to press their presumptive boring tissue (the pedal mantle) against pH-sensing foils, we show that this tissue lowers the pH of surfaces it contacts by greater than or equal to 2 pH units below seawater pH day and night. Acid secretion is likely mediated by vacuolar-type H+-ATPase, which we demonstrate (by immunofluorescence) is abundant in the pedal mantle outer epithelium. Our discovery of acid secretion solves this decades-old mystery and reveals that, during bioerosion, T. crocea can liberate reef constituents directly to the soluble phase, rather than producing sediment alone as earlier assumed.

SUBMITTER: Hill RW

PROVIDER: S-EPMC6030592 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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Acid secretion by the boring organ of the burrowing giant clam, Tridacna crocea.

Hill Richard W RW Armstrong Eric J EJ Inaba Kazuo K Morita Masaya M Tresguerres Martin M Stillman Jonathon H JH Roa Jinae N JN Kwan Garfield T GT

Biology letters 20180601 6

The giant clam Tridacna crocea, native to Indo-Pacific coral reefs, is noted for its unique ability to bore fully into coral rock and is a major agent of reef bioerosion. However, T. crocea's mechanism of boring has remained a mystery despite decades of research. By exploiting a new, two-dimensional pH-sensing technology and manipulating clams to press their presumptive boring tissue (the pedal mantle) against pH-sensing foils, we show that this tissue lowers the pH of surfaces it ...[more]

PMID: 29899125

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Project description:BACKGROUND:Giant clams and scleractinian (reef-building) corals are keystone species of coral reef ecosystems. The basis of their ecological success is a complex and fine-tuned symbiotic relationship with microbes. While the effect of environmental change on the composition of the coral microbiome has been heavily studied, we know very little about the composition and sensitivity of the microbiome associated with clams. Here, we explore the influence of increasing temperature on the microbial community (bacteria and dinoflagellates from the family Symbiodiniaceae) harbored by giant clams, maintained either in isolation or exposed to other reef species. We created artificial benthic assemblages using two coral species (Pocillopora damicornis and Acropora cytherea) and one giant clam species (Tridacna maxima) and studied the microbial community in the latter using metagenomics. RESULTS:Our results led to three major conclusions. First, the health status of giant clams depended on the composition of the benthic species assemblages. Second, we discovered distinct microbiotypes in the studied T. maxima population, one of which was disproportionately dominated by Vibrionaceae and directly linked to clam mortality. Third, neither the increase in water temperature nor the composition of the benthic assemblage had a significant effect on the composition of the Symbiodiniaceae and bacterial communities of T. maxima. CONCLUSIONS:Altogether, our results suggest that at least three microbiotypes naturally exist in the studied clam populations, regardless of water temperature. These microbiotypes plausibly provide similar functions to the clam host via alternate molecular pathways as well as microbiotype-specific functions. This redundancy in functions among microbiotypes together with their specificities provides hope that giant clam populations can tolerate some levels of environmental variation such as increased temperature. Importantly, the composition of the benthic assemblage could make clams susceptible to infections by Vibrionaceae, especially when water temperature increases. Video abstract.

Project description:Molluscan shells are among the most fascinating research objects because of their diverse morphologies and textures. The formation of these delicate biomineralized structures is a matrix-mediated process. A question that arises is what are the essential components required to build these exoskeletons. In order to understand the molecular mechanisms of molluscan shell formation, it is crucial to identify organic macromolecules in different shells from diverse taxa. In the case of bivalves, however, taxon sampling in previous shell proteomics studies are focused predominantly on representatives of the class Pteriomorphia such as pearl oysters, edible oysters and mussels. In this study, we have characterized the shell organic matrix from the crocus clam, Tridacna crocea, (Heterodonta) using various biochemical techniques, including SDS-PAGE, FT-IR, monosaccharide analysis, and enzyme-linked lectin assay (ELLA). Furthermore, we have identified a number of shell matrix proteins (SMPs) using a comprehensive proteomics approach combined to RNA-seq. The biochemical studies confirmed the presence of proteins, polysaccharides, and sulfates in the T. crocea shell organic matrix. Proteomics analysis revealed that the majority of the T. crocea SMPs are novel and dissimilar to known SMPs identified from the other bivalve species. Meanwhile, the SMP repertoire of the crocus clam also includes proteins with conserved functional domains such as chitin-binding domain, VWA domain, and protease inhibitor domain. We also identified BMSP (Blue Mussel Shell Protein, originally reported from Mytilus), which is widely distributed among molluscan shell matrix proteins. Tridacna SMPs also include low-complexity regions (LCRs) that are absent in the other molluscan genomes, indicating that these genes may have evolved in specific lineage. These results highlight the diversity of the organic molecules - in particular proteins - that are essential for molluscan shell formation.

Dataset Information

Acid secretion by the boring organ of the burrowing giant clam, Tridacna crocea.

Publications

Acid secretion by the boring organ of the burrowing giant clam, <i>Tridacna crocea</i>.

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