Deciphering a marine bone degrading microbiome reveals a complex community effort

Borchert, Erik; García-Moyano, Antonio; Sánchez-Carrillo, Sergio; Dahlgren, Thomas G.; Slaby, Beate M.; Bjerga, Gro Elin Kjæreng; Ferrer, Manuel; Franzenburg, Sören; Hentschel, Ute

doi:10.1101/2020.05.13.093005

Cited by 6 publications

(8 citation statements)

References 115 publications

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“…Compared to symbiotic Vestimentifera and asymbiotic annelids, O. frankpressi shows a fast evolving (32), divergent gene repertoire, with gene losses and expansions in key functional groups that support metabolic adaptations to its symbiotic lifestyle (Figure 2, 4A; Supplementary Figure 4D, F). As observed in the marine microbial assemblages on bone surfaces (48), the expansion of secreted matrix metalloproteases (Figure 5A) (29) combined with the active secretion of acid in the root tissue (28) are the most probable mechanisms of bone digestion by the host (Figure 9A). The Osedax-microbe association, however, entails a nutritionally unbalanced diet, being deficient in carbohydrates, but enriched in lipids and proline-and glycine-rich proteins (41, 42) (Figure 9A).…”

Section: Discussionmentioning

confidence: 87%

“…As a core component of vertebrate bones, collagen is poised to be a key nutrient for Osedax (23,25,28) and the bone-associated microbiome (48). Accordingly, transcriptomic analyses uncovered numerous metalloproteases expressed in the root tissue of O. japonicus (29), and our gene family evolutionary analyses showed that genes involved in collagen catabolism and extracellular matrix organisation are expanded in the genome of O. frankpressi (Figure 2H; Supplementary Figure 4F).…”

Section: Osedax Exhibits Lineage-specific Expansions Of Matrix Metall...mentioning

confidence: 92%

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The hologenome of Osedax frankpressi reveals the genetic interplay for the symbiotic digestion of vertebrate bone

Moggioli

Panossian

Sun

et al. 2022

Preprint

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The marine annelid Osedax has evolved a unique heterotrophic symbiosis that allows it to feed exclusively on sunken bones. Yet, the genetic and physiological principles sustaining this symbiosis are poorly understood. Here we show that Osedax frankpressi has a small, AT-rich genome shaped by extensive gene loss. While the Oceanospirillales endosymbiont of Osedax is enriched in genes for carbohydrate and nitrogen metabolism, O. frankpressi has undergone genetic changes to accommodate bone digestion, including the expansion of matrix metalloproteases, and a loss of pathways to synthesize amino acids that are abundant in collagen. Unlike other symbioses, however, innate immunity genes required to acquire and control the endosymbionts are reduced in O. frankpressi. These findings reveal Osedax has evolved an alternative genomic toolkit to bacterial symbiosis where host-symbiont co-dependence has favoured genome simplicity in the host to exploit the nutritionally unbalanced diet of bones.

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Section: Discussionmentioning

confidence: 87%

Section: Osedax Exhibits Lineage-specific Expansions Of Matrix Metall...mentioning

confidence: 92%

The hologenome of Osedax frankpressi reveals the genetic interplay for the symbiotic digestion of vertebrate bone

Moggioli

Panossian

Sun

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…Compared to symbiotic Vestimentifera and asymbiotic annelids, O. frankpressi shows a fast evolving 32 , divergent gene repertoire, with gene losses and expansions in key functional groups that support metabolic adaptations to its symbiotic lifestyle (Figure 2, 4A; Supplementary Figure 4D, F). As observed in the marine microbial assemblages on bone surfaces 48 , the expansion of secreted matrix metalloproteases 29 (Figure 5A) combined with the active secretion of acid in the root tissue 28 are the most probable mechanisms of bone digestion by the host (Figure 9A). The Osedaxmicrobe association, however, entails a nutritionally unbalanced diet, being deficient in carbohydrates, but enriched in lipids and proline-and glycine-rich proteins 41,42 (Figure 9A).…”

Section: Discussionmentioning

confidence: 88%

“…As a core component of vertebrate bones, collagen is poised to be a key nutrient for Osedax 23,25,28 and the bone-associated microbiome 48 . Accordingly, transcriptomic analyses uncovered numerous metalloproteases expressed in the root tissue of O. japonicus 29 , and our gene family evolutionary analyses showed that genes involved in collagen catabolism and extracellular matrix organisation are expanded in the genome of O. frankpressi (Figure 2H; Supplementary Figure 4F).…”

Section: Lineage-specific Expansions Of Matrix Metalloproteinasesmentioning

confidence: 99%

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

Martín-Durán

Moggioli

Panossian

et al. 2022

Preprint

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Annelids have repeatedly evolved symbioses that allow them to colonise extreme ecological niches, like hydrothermal vents and whale falls. Yet, the genetic principles sustaining these symbiotic lifestyles remain unclear. Here we show that different genomic adaptations underpin the symbioses of phylogenetically related annelids with distinct nutritional strategies. While genome compaction and extensive gene losses distinguish the heterotrophic symbiosis of the bone-eating worm Osedax frankpressi, gene gains define the chemoautotrophic symbiosis of deep-sea Vestimentifera. Endosymbionts ultimately compensate most metabolic deficiencies of the host, which include the loss of pathways to recycle nitrogen and synthesise carbohydrates and amino acids enriched in bones in O. frankpressi. Unlike in chemoautotrophic symbioses, innate immunity genes to acquire and control endosymbionts are reduced in O. frankpressi, which, however, has a unique expansion of matrix metalloproteases to digest collagen. Altogether, our study supports that the type of nutritional interaction influences host genome evolution in highly specialized symbioses.

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“…In fact, in the 1500 m samples, WH and WO communities tended to have lower microbial richness and diversity, in comparison to the control SY. WH and WO communities were enriched with organisms related to organic matter decay, as well as chemolithoautotrophic groups (from Campilobacterota and Proteobacteria phyla) (Borchert et al 2020). In addition, there was an increase in Actinobacterota in WO, known for the capabilities to degrade recalcitrant organic matter (Bull et al 2005; Steger et al 2007).…”

Section: Discussionmentioning

confidence: 99%

Development of chemosynthetic microbial communities in organic falls deployed in the deep Southwest Atlantic Ocean

Amendola

Peres²,

Moreira³

et al. 2021

Preprint

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The assembly and successional processes of microbial communities inhabiting deep-sea whale and wood falls are highly complex and vastly unknown, as a myriad of factors may affect the development of a chemosynthetic-based ecosystem on these organic islands. The chemoautotrophy supported by organic substrates is the basis of long-lasting ecosystems, considered biodiversity hotspots in the oligotrophic deep sea. Understanding how these microbial communities develop and the factors affecting them could shed light on processes related to the maintenance of biodiversity in this environment. We performed a whale- and wood-fall experiment in the southwest Atlantic on the Brazilian continental margin and investigated biofilm-forming bacterial and archaeal communities colonising these substrates, deployed at 1500 and 3300 m depth. The composition of the prokaryotic communities shared some similarities with previously reported organic falls in the north Pacific and the Mediterranean Sea, mainly regarding sulphur oxidising chemolithotrophic taxa from the phyla Campylobacterota and Proteobacteria. Communities were found to be highly different between the organic substrates, as whale fall associated biofilms presented a higher dominance of sulphur oxidising chemolithotrophs. We also observed a significant difference between the two sites, with the whale associated communities at the 1500 isobath presenting a faster establishment of the chemosynthetic taxa.

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Deciphering a marine bone degrading microbiome reveals a complex community effort

Abstract: word count: 250 1 7 Text word count: 4926 (excluding Abstract, Importance, Materials and Methods) 1 8 Abstract 1 9

Cited by 6 publications

References 115 publications

The hologenome of Osedax frankpressi reveals the genetic interplay for the symbiotic digestion of vertebrate bone

The hologenome of Osedax frankpressi reveals the genetic interplay for the symbiotic digestion of vertebrate bone

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

Development of chemosynthetic microbial communities in organic falls deployed in the deep Southwest Atlantic Ocean

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