The inner mantle of the giant clam, Tridacna squamosa, expresses a basolateral Na+/K+-ATPase α-subunit, which displays light-dependent gene and protein expression along the shell-facing epithelium

Boo, Mel V.; Hiong, Kum C.; Choo, Celine Yen Ling; Cao-Pham, Anh H.; Wong, Wai P.; Chew, Shit F.; Ip, Yuen K.

doi:10.1371/journal.pone.0186865

Cited by 20 publications

(8 citation statements)

References 66 publications

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“…The gills of giant clams have been previously shown to be responsible for the uptake and assimilation of ammonia from the surrounding seawater (Rees et al, 1994; Shepherd et al, 1999). The ability of assimilating exogenous ammonia and recycling nitrogen between the giant clam host and their symbionts is assumed to be reason for the success of Tridacninae in the oligotrophic waters of tropical oceans (Boo et al, 2017). The strong association of Endozoicomonadaceae with giant clam gill tissues could therefore be an indication for the contribution of this bacterial group to processes related to nitrogen uptake.…”

Section: Discussionmentioning

confidence: 99%

Tissue-Specific Microbiomes of the Red Sea Giant Clam Tridacna maxima Highlight Differential Abundance of Endozoicomonadaceae

et al. 2019

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Giant clams (subfamily Tridacninae) are prevalent members of coral reef communities and engage in symbioses with algal photosymbionts of the family Symbiodiniaceae, similar to their scleractinian coral counterparts. However, we know little about their associated bacterial microbiome members. Here, we explored bacterial community diversity of digestive system, gill, and mantle tissues associated with the giant clam Tridacna maxima across a cross-shelf gradient (inshore, midshore, and offshore reef sites) in the central Red Sea using 16S rRNA gene amplicon sequencing. Different tissues harbor spatially stable and distinct microbial communities. Notably, diverse assemblages of bacteria affiliated to the family Endozoicomonadaceae were prevalent in all tissues, but particularly abundant in gills and to a lesser extent in digestive tissues. Besides Endozoicomonadaceae, bacteria in the families Pasteurellaceae, Alteromonadaceae, and Comamonadaceae were common associates, depending on the tissue queried. Taxonomy-based functional inference identified processes related to nitrogen cycling (among others) to be enriched in giant clam tissues and contributed by Endozoicomonadaceae. Our study highlights the tissue-specificity and broad taxonomic range of Endozoicomonadaceae associates, similar to other marine invertebrates, and suggests their contribution to nitrogen-related pathways. The investigation of bivalve-associated microbiome communities provides an important addition to the pathogen-focused studies for commercially important bivalves (e.g., oysters).

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Section: Discussionmentioning

confidence: 99%

Tissue-Specific Microbiomes of the Red Sea Giant Clam Tridacna maxima Highlight Differential Abundance of Endozoicomonadaceae

et al. 2019

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“…The apical Na + /Ca 2+ exchanger 3 (NCX3) in the shell-facing inner mantle epithelium can deliver Ca 2+ to the extrapallial fluid at a high rate (Boo et al, 2019), while the apical PMCA can function to fine-tune cytosolic [Ca 2+ ] (Ip et al, 2018). The operation of NCX3 requires the support of Na + /K + -ATPase (NKA; Boo et al, 2017), and the movement of Ca 2+ inside the epithelial cells needs the participation of Sarcoplasmic Reticulum Ca 2+ -ATPase (SERCA; . ER, endoplasmic reticulum.…”

Section: The Inner Mantle Participates In Light-enhanced Shell Formationmentioning

confidence: 99%

“…The cDNA coding sequence of NKA α-subunit (NKAα) has been obtained from the inner mantle of T. squamosa (Boo et al, 2017). NKAα has a basolateral localization along the shell-facing epithelium of the inner mantle, and there is a significantly stronger basolateral NKAα-immunofluorescence at the shellfacing epithelium of individuals exposed to light for 12 h than that of the control (Boo et al, 2017). In addition, illumination leads to a significant increase in the protein abundance of NKAα in the inner mantle (Table 1).…”

Section: The Inner Mantle Participates In Light-enhanced Shell Formationmentioning

confidence: 99%

Light-Dependent Phenomena and Related Molecular Mechanisms in Giant Clam-Dinoflagellate Associations: A Review

Chew

2021

Front. Mar. Sci.

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Giant clams can grow to large sizes despite living in oligotrophic waters of the tropical Indo-Pacific as they maintain a mutualistic relationship with symbiotic dinoflagellates (zooxanthellae) and receive photosynthate from them. The phototrophic dinoflagellates live extracellularly inside a tubular system located mainly in the colorful outer mantle and have no access to the ambient seawater. Hence, the clam host needs to absorb exogenous inorganic carbon (Ci), nitrogen (N) and phosphorus (P), and supply them to the symbionts. As photosynthesizing symbionts need more nutrients in light than in the dark, the uptake rates of these exogenous nutrients by the host must increase during illumination, implying that the host’s transporters involved need to be regulated by some kind of light-responsive mechanisms. Furthermore, the growth and development of the host can also be augmented by light, because of the photosynthate donated by the photosynthesizing symbionts. Consequently, giant clams display many light-dependent phenomena related to phototrophy, antioxidative defense, biomineralization, as well as absorption of exogenous Ci, N, and P. These phenomena may involve collaborations among enzymes and transporters in several organs of the host, whereby the gene and protein expression levels of these biocatalysts are up- or down-regulated during illumination. This review aims to examine the molecular mechanisms of light-dependent physiological phenomena that occur in intact giant clam-dinoflagellate associations, and to highlight the differences between giant clams and scleractinian corals in those regards. As the population of giant clams in nature are dwindling due to climate change and anthropogenic activities, a good understanding of their light-dependent processes may generate new ideas to improve their growth and survival under rapidly changing environmental conditions.

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“…However, other enzymes and transporters, some of which unrelated to

, also display light-enhanced gene and/or protein expression in T. squamosa . These include the Glutamine Synthetase (Hiong et al, 2017a ), the NHE3-like (Hiong et al, 2017b ), and the urea active transporter DUR3-like (Chan et al, 2018 ) of the ctenidium as well as the Plasma Membrane Ca 2+ -ATPase (Ip et al, 2017a ) and the Na + /K + -ATPase α-subunit (Boo et al, 2017 ) of the inner mantle. Hence, it is logical to conclude that T. squamosa may have developed a general mechanism to coordinate the expression levels of a variety of enzymes and transporters in relation to various diurnally light-dependent physiological processes, including light-enhanced C i absorption, light-enhanced ammonia absorption and assimilation, and light-enhanced calcification.…”

Section: Discussionmentioning

confidence: 99%

Molecular Characterization of a Dual Domain Carbonic Anhydrase From the Ctenidium of the Giant Clam, Tridacna squamosa, and Its Expression Levels After Light Exposure, Cellular Localization, and Possible Role in the Uptake of Exogenous Inorganic Carbon

et al. 2018

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A Dual-Domain Carbonic Anhydrase (DDCA) had been sequenced and characterized from the ctenidia (gills) of the giant clam, Tridacna squamosa, which lives in symbiosis with zooxanthellae. DDCA was expressed predominantly in the ctenidium. The complete cDNA coding sequence of DDCA from T. squamosa comprised 1,803 bp, encoding a protein of 601 amino acids and 66.7 kDa. The deduced DDCA sequence contained two distinct α-CA domains, each with a specific catalytic site. It had a high sequence similarity with tgCA from Tridacna gigas. In T. squamosa, the DDCA was localized apically in certain epithelial cells near the base of the ctenidial filament and the epithelial cells surrounding the tertiary water channels. Due to the presence of two transmembrane regions in the DDCA, one of the Zn2+-containing active sites could be located externally and the other one inside the cell. These results denote that the ctenidial DDCA was positioned to dehydrate HCO3- to CO2 in seawater, and to hydrate the CO2 that had permeated the apical membrane back to HCO3- in the cytoplasm. During insolation, the host clam needs to increase the uptake of inorganic carbon from the ambient seawater to benefit the symbiotic zooxanthellae; only then, can the symbionts conduct photosynthesis and share the photosynthates with the host. Indeed, the transcript and protein levels of DDCA/DDCA in the ctenidium of T. squamosa increased significantly after 6 and 12 h of exposure to light, respectively, denoting that DDCA could participate in the light-enhanced uptake and assimilation of exogenous inorganic carbon.

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The inner mantle of the giant clam, Tridacna squamosa, expresses a basolateral Na+/K+-ATPase α-subunit, which displays light-dependent gene and protein expression along the shell-facing epithelium

Cited by 20 publications

References 66 publications

Tissue-Specific Microbiomes of the Red Sea Giant Clam Tridacna maxima Highlight Differential Abundance of Endozoicomonadaceae

Tissue-Specific Microbiomes of the Red Sea Giant Clam Tridacna maxima Highlight Differential Abundance of Endozoicomonadaceae

Light-Dependent Phenomena and Related Molecular Mechanisms in Giant Clam-Dinoflagellate Associations: A Review

Molecular Characterization of a Dual Domain Carbonic Anhydrase From the Ctenidium of the Giant Clam, Tridacna squamosa, and Its Expression Levels After Light Exposure, Cellular Localization, and Possible Role in the Uptake of Exogenous Inorganic Carbon

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