Distinct genomic routes underlie transitions to specialised symbiotic lifestyles in deep-sea annelid worms

Abstract

Bacterial symbioses allow annelids to colonise extreme ecological niches, such as hydrothermal vents and whale falls. Yet, the genetic principles sustaining these symbioses remain unclear. Here, we show that different genomic adaptations underpin the symbioses of phylogenetically related annelids with distinct nutritional strategies. Genome compaction and extensive gene losses distinguish the heterotrophic symbiosis of the bone-eating worm Osedax frankpressi from the chemoautotrophic symbiosis of deep-sea Vestimentifera. Osedax’s endosymbionts complement many of the host’s metabolic deficiencies, including the loss of pathways to recycle nitrogen and synthesise some amino acids. Osedax’s endosymbionts possess the glyoxylate cycle, which could allow more efficient catabolism of bone-derived nutrients and the production of carbohydrates from fatty acids. Unlike in most Vestimentifera, innate immunity genes are reduced in O. frankpressi, which, however, has an expansion of matrix metalloproteases to digest collagen. Our study supports that distinct nutritional interactions influence host genome evolution differently in highly specialised symbioses.

Third-Generation Sequencing Reveals the Adaptive Role of the Epigenome in Three Deep-Sea Polychaetes

“… f Patra et al (in prep). g Moggioli et al (2023) . h Data available at https://phaidra.univie.ac.at/detail/o:1220865 .…”

“…Lastly, two genes for the methionine adenosyltransferases (MATa and MATb) were found in both the tubeworms and alvinellid species ( supplementary table S4, Supplementary Material online). Recent genetic and transcriptomic data revealed two versions of MAT also exist in the Alvinellidae's sister group Amphraetidae ( Stiller et al 2020 ), Osedax ( Moggioli et al 2023 ), and some species of the Terebellidae family ( supplementary fig. S3, Supplementary Material online).…”

GC content across insect genomes: phylogenetic patterns, causes and consequences

“…Theoretically, a trend towards increasing genome-wide AT content could be caused by modification to any of these processes. The deep-sea bone-eating polychaete worm Osedax frankpressi has an AT-rich genome similar to that of Bombylius (GC content 29%; Moggioli et al, 2023). In this case, an underlying cause is proposed to be loss of genes encoding components of the BER pathway, including SMUG1 which recognizes U:G base pairs resulting from C deamination (Krokan and Bjørås, 2013; Moggioli et al, 2023).…”

“…The deep-sea bone-eating polychaete worm Osedax frankpressi has an AT-rich genome similar to that of Bombylius (GC content 29%; Moggioli et al, 2023). In this case, an underlying cause is proposed to be loss of genes encoding components of the BER pathway, including SMUG1 which recognizes U:G base pairs resulting from C deamination (Krokan and Bjørås, 2013; Moggioli et al, 2023). However, we suggest this may not be the underlying cause in bee-flies, since we found homologues of BER genes missing from Osedax , including smug1 , tdg and ogg1 , in Bombylius and all flies in our data set (Supplementary Figure S3).…”

Reduced chemosymbiont genome in the methane seep thyasirid and the cooperated metabolisms in the holobiont under anaerobic sediment

“…Haima. The active V-type H +transporting ATPase would create an acid micro-environment in lysosome for the digestion(Marshansky & Futai, 2008;Moggioli et al, 2023), with 10 of 13 subunits expressing more than 100 TPM. Cathepsins, the critical enzyme for digestion in the lysosome, were highly expressed in the host gill tissue, including CathepsinB, C, D, F, L and X, ranging from 153 to 2393 TPM.…”