Proteins in the Crystalline Styles of the Marine Mussels<i>Perna canaliculus</i>Gmelin and<i>Mytilus galloprovincialis</i>Lamarck

MacKenzie, A. Lincoln; Marshall, Craig J.

doi:10.2983/035.033.0302

Cited by 6 publications

(3 citation statements)

References 40 publications

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“…The crystalline style, found in bivalve molluscs and some gastropods, is an acellular rod rich in glycoproteins, located inside the crystalline style sac [ 34 ] (Fig. 2 D,E).…”

Section: Resultsmentioning

confidence: 99%

Characterisation of the enzyme transport path between shipworms and their bacterial symbionts

et al. 2021

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Background Shipworms are marine xylophagus bivalve molluscs, which can live on a diet solely of wood due to their ability to produce plant cell wall-degrading enzymes. Bacterial carbohydrate-active enzymes (CAZymes), synthesised by endosymbionts living in specialised shipworm cells called bacteriocytes and located in the animal’s gills, play an important role in wood digestion in shipworms. However, the main site of lignocellulose digestion within these wood-boring molluscs, which contains both endogenous lignocellulolytic enzymes and prokaryotic enzymes, is the caecum, and the mechanism by which bacterial enzymes reach the distant caecum lumen has remained so far mysterious. Here, we provide a characterisation of the path through which bacterial CAZymes produced in the gills of the shipworm Lyrodus pedicellatus reach the distant caecum to contribute to the digestion of wood. Results Through a combination of transcriptomics, proteomics, X-ray microtomography, electron microscopy studies and in vitro biochemical characterisation, we show that wood-digesting enzymes produced by symbiotic bacteria are localised not only in the gills, but also in the lumen of the food groove, a stream of mucus secreted by gill cells that carries food particles trapped by filter feeding to the mouth. Bacterial CAZymes are also present in the crystalline style and in the caecum of their shipworm host, suggesting a unique pathway by which enzymes involved in a symbiotic interaction are transported to their site of action. Finally, we characterise in vitro four new bacterial glycosyl hydrolases and a lytic polysaccharide monooxygenase identified in our transcriptomic and proteomic analyses as some of the major bacterial enzymes involved in this unusual biological system. Conclusion Based on our data, we propose that bacteria and their enzymes are transported from the gills along the food groove to the shipworm’s mouth and digestive tract, where they aid in wood digestion.

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“…The crystalline style, found in bivalve molluscs and some gastropods, is an acellular rod rich in glycoproteins, located inside the crystalline style sac [ 34 ] (Fig. 2 D,E).…”

Section: Resultsmentioning

confidence: 99%

Characterisation of the enzyme transport path between shipworms and their bacterial symbionts

et al. 2021

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“…The extension of the crystalline style, from a position ventral to and near the anterior end of the foot to a position well posterior to the shell valves, is unique to Tamilokus (Turner, 1966). In other bivalves, cilia-mediated rotation of the crystalline style is thought to aid digestion by mixing enzymes and reducing food particle size through mechanical action (Robin et al, 2018; Nelson, 1918; Edmondson, 1920; Yonge, 1923; Lavine, 1946; Morton, 1952; Horiuchi & Lane, 1982; Alyakrinskaya, 2001; Sakamoto et al, 2008; Mackenzie & Marshall, 2014). However, the functional significance of the exceptionally large style of Tamilokus remains to be explained.…”

Section: Discussionmentioning

confidence: 99%

Tamilokus mabinia, a new, anatomically divergent genus and species of wood-boring bivalve from the Philippines

Shipway

Altamia

Rosenberg

et al. 2019

PeerJ

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Here we describe an anatomically divergent wood-boring bivalve belonging to the family Teredinidae. Specimens were collected off the coast of Mabini, Batangas, Philippines, in February 2018, from sunken driftwood at a depth of less than 2 m. A combination of characteristics differentiates these specimens from members of previously named teredinid genera and species. Most notable among these include: an enlarged cephalic hood which extends across the posterior slope of the shell valves and integrates into the posterior adductor muscle; a unique structure, which we term the ‘cephalic collar’, formed by protruding folds of the mantle immediately ventral to the foot and extending past the posterior margin of the valves; a large globular stomach located entirely posterior to the posterior adductor muscle and extending substantially beyond the posterior gape of the valves; an elongate crystalline style and style sac extending from the base of the foot, past the posterior adductor muscle, to the posteriorly located stomach; calcareous pallets distinct from those of described genera; a prominently flared mantle collar which extends midway along the stalk of the pallets; and, separated siphons that bear a pigmented pinstripe pattern with highly elaborate compound papillae on the incurrent siphon aperture. We used Micro-Computed Tomography (Micro-CT) to build a virtual 3D anatomical model of this organism, confirming the spatial arrangement of the structures described above. Phylogenetic analysis of the small (18S) and large (28S) nuclear rRNA gene sequences, place this bivalve within the Teredindae on a branch well differentiated from previously named genera and species. We propose the new genus and species Tamilokus mabinia to accommodate these organisms, raising the total number of genera in this economically and environmentally important family to 17. This study demonstrates the efficacy of Micro-CT for anatomical description of a systematically challenging group of bivalves whose highly derived body plans are differentiated predominantly by soft tissue adaptations rather than features of calcareous hard-parts.

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“…The apex of the style (Fig. 14, apx) projects from the crystalline style sac into the stomach, where it presses and rotates against the gastric shield, a chitinous structure in the surface of the stomach (MacKenzie et al 2014). In other fcw folded caecum wall, mvb microvillar border, ga Golgi apparatus, w wood bivalves, it was observed that the style dissolves partially releasing enzymes only when organisms are feeding (Kristensen 1972).…”

Section: Stomach Caecum Digestive Gland and Intestinementioning

confidence: 99%

A picture is worth a thousand words: novel photographic evidence on the anatomy of the digestive system of three shipworm species (Bivalvia, Teredinidae)

Borges¹,

Pfeifer

Pandur

et al. 2021

Zoomorphology

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Adult shipworms (Bivalvia, Teredinidae) have greatly elongate bodies, and thus, the organs have a different orientation than those of other bivalves. Studies on the anatomy of the digestive system have been carried out in a number of genera and species in the Teredinidae, but are now over 50 years old and most were carried in only a few preserved specimens. These studies contain descriptions and line drawings, but high-resolution images do not exist, except for Lyrodus pedicellatus that was recently studied using modern techniques. Thus, we present high-resolution images of fresh specimens of three teredinid species, representing three genera, to show the different features of each organ of the digestive tract and intra-and inter-specific differences. Most of our observations concur with, but some differ from previous descriptions. One observation in Teredo navalis showed, for the first time, the foot covered by a membrane with corrugated aspect, which the function is not yet understood. Another observation in the same species showed that the caecum and intestine have strikingly different colourations in specimens in overcrowded conditions when compared with those in uncrowded conditions. This may indicate that the former resort more to filter feeding to avoid the complete destruction of their habitat. In Psiloteredo megotara, the digestive gland seems to cover the caecum, as it does in Nototeredo norvagica and differing from a previous line drawing for the former species. Faecal pellets were observed in N. norvagica and P. megotara, which may indicate a more complete utilization of wood in these species.

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Proteins in the Crystalline Styles of the Marine MusselsPerna canaliculusGmelin andMytilus galloprovincialisLamarck

Cited by 6 publications

References 40 publications

Characterisation of the enzyme transport path between shipworms and their bacterial symbionts

Characterisation of the enzyme transport path between shipworms and their bacterial symbionts

Tamilokus mabinia, a new, anatomically divergent genus and species of wood-boring bivalve from the Philippines

A picture is worth a thousand words: novel photographic evidence on the anatomy of the digestive system of three shipworm species (Bivalvia, Teredinidae)

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