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Comparative proteomics of related symbiotic mussel species reveals high variability of host-symbiont interactions.

ABSTRACT: Deep-sea Bathymodiolus mussels and their chemoautotrophic symbionts are well-studied representatives of mutualistic host-microbe associations. However, how host-symbiont interactions vary on the molecular level between related host and symbiont species remains unclear. Therefore, we compared the host and symbiont metaproteomes of Pacific B. thermophilus, hosting a thiotrophic symbiont, and Atlantic B. azoricus, containing two symbionts, a thiotroph and a methanotroph. We identified common strategies of metabolic support between hosts and symbionts, such as the oxidation of sulfide by the host, which provides a thiosulfate reservoir for the thiotrophic symbionts, and a cycling mechanism that could supply the host with symbiont-derived amino acids. However, expression levels of these processes differed substantially between both symbioses. Backed up by genomic comparisons, our results furthermore revealed an exceptionally large repertoire of attachment-related proteins in the B. thermophilus symbiont. These findings imply that host-microbe interactions can be quite variable, even between closely related systems.

SUBMITTER: Ponnudurai R

PROVIDER: S-EPMC6976577 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Comparative proteomics of related symbiotic mussel species reveals high variability of host-symbiont interactions.

Ponnudurai Ruby R Heiden Stefan E SE Sayavedra Lizbeth L Hinzke Tjorven T Kleiner Manuel M Hentschker Christian C Felbeck Horst H Sievert Stefan M SM Schlüter Rabea R Becher Dörte D Schweder Thomas T Markert Stephanie S

The ISME journal 20191104 2

Deep-sea Bathymodiolus mussels and their chemoautotrophic symbionts are well-studied representatives of mutualistic host-microbe associations. However, how host-symbiont interactions vary on the molecular level between related host and symbiont species remains unclear. Therefore, we compared the host and symbiont metaproteomes of Pacific B. thermophilus, hosting a thiotrophic symbiont, and Atlantic B. azoricus, containing two symbionts, a thiotroph and a methanotroph. We identified common strate ...[more]

PMID: 31680119

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Project description:BackgroundHost-symbiont co-speciation and reductive genome evolution have been commonly observed among obligate endocellular insect symbionts, while such examples have rarely been identified among extracellular ones, the only case reported being from gut symbiotic bacteria of stinkbugs of the family Plataspidae. Considering that gut symbiotic communities are vulnerable to invasion of foreign microbes, gut symbiotic associations have been thought to be evolutionarily not stable. Stinkbugs of the family Acanthosomatidae harbor a bacterial symbiont in the midgut crypts, the lumen of which is completely sealed off from the midgut main tract, thereby retaining the symbiont in the isolated cryptic cavities. We investigated histological, ecological, phylogenetic, and genomic aspects of the unique gut symbiosis of the acanthosomatid stinkbugs.ResultsPhylogenetic analyses showed that the acanthosomatid symbionts constitute a distinct clade in the gamma-Proteobacteria, whose sister groups are the obligate endocellular symbionts of aphids Buchnera and the obligate gut symbionts of plataspid stinkbugs Ishikawaella. In addition to the midgut crypts, the symbionts were located in a pair of peculiar lubricating organs associated with the female ovipositor, by which the symbionts are vertically transmitted via egg surface contamination. The symbionts were detected not from ovaries but from deposited eggs, and surface sterilization of eggs resulted in symbiont-free hatchlings. The symbiont-free insects suffered retarded growth, high mortality, and abnormal morphology, suggesting important biological roles of the symbiont for the host insects. The symbiont phylogeny was generally concordant with the host phylogeny, indicating host-symbiont co-speciation over evolutionary time despite the extracellular association. Meanwhile, some local host-symbiont phylogenetic discrepancies were found, suggesting occasional horizontal symbiont transfers across the host lineages. The symbionts exhibited AT-biased nucleotide composition, accelerated molecular evolution, and reduced genome size, as has been observed in obligate endocellular insect symbionts.ConclusionComprehensive studies of the acanthosomatid bacterial symbiosis provide new insights into the genomic evolution of extracellular symbiotic bacteria: host-symbiont co-speciation and drastic genome reduction can occur not only in endocellular symbiotic associations but also in extracellular ones. We suggest that many more such cases might be discovered in future surveys.

Project description:The ability of certain Pseudomonas (P.) species to grow or persist in anoxic habitats by either denitrification, acetate fermentation, or arginine fermentation has been described in several studies as a special property. Previously, we had isolated strains belonging to the species P. lundensis, P. weihenstephanensis, and P. fragi from anoxic modified atmosphere packaged (MAP) minced beef and further proved their anaerobic growth in vitro on agar plates. This follow-up study investigated the anaerobic growth of two strains per respective species in situ on inoculated chicken breast filet under 100% N2 modified atmosphere. We were able to prove anaerobic growth of all six strains on chicken breast filet with cell division rates of 0.2-0.8/day. Furthermore, we characterized the anaerobic metabolic lifestyle of these Pseudomonas strains by comparative proteomics, upon their cultivation in meat simulation media, which were constantly gassed with either air or 100% N2 atmospheres. From these proteomic predictions, and respective complementation by physiological experiments, we conclude that the Pseudomonas strains P. fragi, P. weihenstephanensis, P. lundensis exhibit a similar anaerobic lifestyle and employ arginine fermentation via the arginine deiminase (ADI) pathway to grow anaerobically also on MAP meats. Furthermore, glucose fermentation to ethanol via the ED-pathway is predicted to enable long term survival but no true growth, while respiratory growth with nitrate as alternative electron acceptor or glucose fermentation to acetate could be excluded due to absence of essential genes. The citric acid cycle is partially bypassed by the glyoxylate shunt, functioning as the gluconeogenetic route without production of NADH2 under carbon limiting conditions as e.g., in packaged meats. Triggered by an altered redox balance, we also detected upregulation of enzymes involved in protein folding as well as disulfide bonds isomerization under anoxic conditions as a counteracting mechanism to reduce protein misfolding. Hence, this study reveals the mechanisms enabling anaerobic grow and persistence of common meat-spoiling Pseudomonas species, and further complements the hitherto limited knowledge of the anaerobic lifestyle of Pseudomonas species in general.

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Comparative proteomics of related symbiotic mussel species reveals high variability of host-symbiont interactions.

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Comparative proteomics of related symbiotic mussel species reveals high variability of host-symbiont interactions.

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