In summary, this cooperative partnership has evolved through time in a complex
relationship in which both sides have deployed a sophisticated signalling communication network to ensure the success of the holobiont.
24.3 Gill Symbionts
An illustrative interaction between bivalve molluscs and microbes takes place in the
molluscan gills. In this organ, environmentally or vertically transmitted symbiotic
bacteria colonise by endocytosis the gill filaments, as the gills are developing, in a
self-infection process (Wentrup et al. 2014). In this association, microbes are
internalised by the host eukaryotic cells and contained inside specialised vesicles
or bacteriocytes. Among the high bacterial diversity in water environments,
chemosymbiotic bacteria have been associated with clam and mussel gills where
they use inorganic chemical energy for the synthesis of organic compounds for the
benefit of their hosts (Fig. 24.1).
For example, methanotrophs and thiotrophs have been reported to be the most
common symbiotic bacteria in Bathymodiolus mussels (Fujiwara et al. 2000), a
bivalve adapted to live in cold seeps and hydrothermal vents. The Bathymodiolus
platifrons species depend on the organic carbon supplied by the symbionts inside
their gills, and the establishment of the endosymbiosis is a crucial step to deep-sea
adaptation in this mussel (Kellermann et al. 2012). However, the presence of these
chemosyntetic symbionts is environmentally dependant in Bathymodiolus mussels
(Duperron et al. 2007; Bettencourt et al. 2008; Yu et al. 2019), and when they are
transferred from a vent to an atmospheric adapted environment the abundance of
symbionts has been observed to decline significantly (Sun et al. 2017). Yu et al.
(2019) found that the lysosomal system of the mussel plays an important role in
controlling the abundance of endosymbionts in the host. They discovered a
lysosomal-related gene, encoding a vesicle-associated membrane protein (VAMP),
which expressed at a high level and presented exactly where the methanotrophs
occurred. Its expression decreases in the absence of methane, thus the presence of
methanotrophs is reduced too.
Gill endosymbionts, which are environmentally acquired, are also present in
Lucinidae clams. Despite their filter-feeding habit, these clams complete their
nutritional needs through obligate chemosymbiotic associations with
gammaproteobacterial endosymbionts inside bacteriocytes in their gills (Taylor
and Glover 2000). Different studies revealed that the main functions of the lucinid
endosymbionts were denitrification, assimilation of nitrogenous compounds and
inorganic carbon fixation for their hosts using energy obtained by the oxidation of
reduced sulfur compounds (Cavanaugh et al. 2006; König et al. 2016; Petersen et al.
2016). A recent study analysed the associated symbionts to the lucinid clam
Phacoides pectinatus by utilising 16S rRNA gene targeting, metagenomics and
metatranscriptomics (Lim et al. 2020). Authors found that the major fraction of the
endosymbionts (84%) was dominated by one gammaproteobacterial
24 Coevolution of Molluscs and Their Microbes
517
relationship in which both sides have deployed a sophisticated signalling communication network to ensure the success of the holobiont.
24.3 Gill Symbionts
An illustrative interaction between bivalve molluscs and microbes takes place in the
molluscan gills. In this organ, environmentally or vertically transmitted symbiotic
bacteria colonise by endocytosis the gill filaments, as the gills are developing, in a
self-infection process (Wentrup et al. 2014). In this association, microbes are
internalised by the host eukaryotic cells and contained inside specialised vesicles
or bacteriocytes. Among the high bacterial diversity in water environments,
chemosymbiotic bacteria have been associated with clam and mussel gills where
they use inorganic chemical energy for the synthesis of organic compounds for the
benefit of their hosts (Fig. 24.1).
For example, methanotrophs and thiotrophs have been reported to be the most
common symbiotic bacteria in Bathymodiolus mussels (Fujiwara et al. 2000), a
bivalve adapted to live in cold seeps and hydrothermal vents. The Bathymodiolus
platifrons species depend on the organic carbon supplied by the symbionts inside
their gills, and the establishment of the endosymbiosis is a crucial step to deep-sea
adaptation in this mussel (Kellermann et al. 2012). However, the presence of these
chemosyntetic symbionts is environmentally dependant in Bathymodiolus mussels
(Duperron et al. 2007; Bettencourt et al. 2008; Yu et al. 2019), and when they are
transferred from a vent to an atmospheric adapted environment the abundance of
symbionts has been observed to decline significantly (Sun et al. 2017). Yu et al.
(2019) found that the lysosomal system of the mussel plays an important role in
controlling the abundance of endosymbionts in the host. They discovered a
lysosomal-related gene, encoding a vesicle-associated membrane protein (VAMP),
which expressed at a high level and presented exactly where the methanotrophs
occurred. Its expression decreases in the absence of methane, thus the presence of
methanotrophs is reduced too.
Gill endosymbionts, which are environmentally acquired, are also present in
Lucinidae clams. Despite their filter-feeding habit, these clams complete their
nutritional needs through obligate chemosymbiotic associations with
gammaproteobacterial endosymbionts inside bacteriocytes in their gills (Taylor
and Glover 2000). Different studies revealed that the main functions of the lucinid
endosymbionts were denitrification, assimilation of nitrogenous compounds and
inorganic carbon fixation for their hosts using energy obtained by the oxidation of
reduced sulfur compounds (Cavanaugh et al. 2006; König et al. 2016; Petersen et al.
2016). A recent study analysed the associated symbionts to the lucinid clam
Phacoides pectinatus by utilising 16S rRNA gene targeting, metagenomics and
metatranscriptomics (Lim et al. 2020). Authors found that the major fraction of the
endosymbionts (84%) was dominated by one gammaproteobacterial
24 Coevolution of Molluscs and Their Microbes
517