Coming together—symbiont acquisition and early development in deep-sea bathymodioline mussels

Abstract

How and when symbionts are acquired by their animal hosts has a profound impact on the ecology and evolution of the symbiosis. Understanding symbiont acquisition is particularly challenging in deep-sea organisms because early life stages are so rarely found. Here, we collected early developmental stages of three deep-sea bathymodioline species from different habitats to identify when these acquire their symbionts and how their body plan adapts to a symbiotic lifestyle. These mussels gain their nutrition from chemosynthetic bacteria, allowing them to thrive at deep-sea vents and seeps worldwide. Correlative imaging analyses using synchrotron-radiation based microtomography together with light, fluorescence and electron microscopy revealed that the pediveliger larvae were aposymbiotic. Symbiont colonization began during metamorphosis from a planktonic to a benthic lifestyle, with the symbionts rapidly colonizing first the gills, the symbiotic organ of adults, followed by all other epithelia of their hosts. Once symbiont densities in plantigrades reached those of adults, the host's intestine changed from the looped anatomy typical for bivalves to a straightened form. Within the Mytilidae, this morphological change appears to be specific to Bathymodiolus and Gigantidas , and is probably linked to the decrease in the importance of filter feeding when these mussels switch to gaining their nutrition largely from their symbionts.

DNA Enrichment Methods for Microbial Symbionts in Marine Bivalves

“…The collection and enrichment of bacteria and archaea from bivalve gills could be performed according to the distinct sizes of the host and microbial cells [23]. Bivalve gill epithelial cells are on average 20 µm wide, whereas a typical bacterial cell is ~2 µm [22]. We accordingly filtrated tissue homogenate across a 40 µm cell strainer and filters with pore sizes of 5 µm [54] to enrich bacteria and archaea cells.…”

“…Due to the important economic value and ecological benefits of bivalves, it is essential to identify the microorganisms in bivalves and uncover their roles. Given many symbiotic microorganisms that cannot be cultivated in vitro, the current research on bivalve symbionts mainly relies on culture-independent technologies including nano-scale secondary ion mass spectrometry (NanoSIMS) [20], high-throughput sequencing [17], matrix-assisted laser desorption/ionization MSI (MALDI-MSI) [21], and synchrotron-radiation based microcomputed tomography (SRµCT) [22]. The widely used high-throughput sequencing technology allows us to investigate the diversity of microorganisms and the mechanisms of symbiosis in mussels without the need for prior cultivation [17,23].…”

Lipid Biomarker Patterns Reflect Nutritional Strategies of Seep-Dwelling Bivalves From the South China Sea

“…Fiala-Médioni et al (2002) suggested the existence of dual symbiosis, providing the host with greater environmental tolerance and increased niche space. Unfortunately, symbiotic bacteria from hydrothermal vents and hydrocarbon seeps have not been cultured successfully to date (Franke et al, 2021). Symbiotic bacteria and their symbiotic associations between hosts and symbionts are typically studied with electron microscopy, enzymatic analyses, 16S rRNA work, as well as lipid biomarkers and their carbon stable isotope compositions (Duperron et al, 2009;Petersen and Dubilier, 2010;Feng et al, 2015).…”

Intracellular Bacterial Symbionts in Corals: Challenges and Future Directions

“…Intracellular symbiosis between eukaryotes and bacteria is widespread across the tree of life and is known from insects [14,15], marine organisms such as bivalves and tubeworms [16,17], plants [18,19], and protists [20]. The intracellular nature of these associations provides multiple advantages.…”