Manuel Kleiner

Diet-derived peptides mediate the effects of dietary protein source on gastrointestinal health

Symbiosis reshapes metabolism of sulfate-reducing bacteria in gutless marine worms.

Sulfate-reducing bacteria (SRB) are widespread in marine and terrestrial environments, where they often form syntrophic associations with bacteria, archaea, and eukaryotes. Among the most intimate of these are multipartite symbioses in gutless marine oligochaete worms, which host SRB and sulfur-oxidizing endosymbionts that engage in a syntrophic exchange of sulfur compounds. Despite decades of research on free-living SRB, the metabolic traits that enable SRB to persist in symbiosis, and how these differ across hosts and environments, remain poorly understood. We show that a globally distributed clade of symbiotic SRB, which we named Candidatus Desulfoconcordia, has a conserved core metabolism that diverges from free-living relatives. Using comparative genomics and metaproteomics, we reveal that these endosymbionts retain key traits of SRB such as sulfate reduction, complete oxidation of acetate to CO2, amino acid degradation for nitrogen acquisition, and transport of essential nutrients. However, they exhibit a more oxygen-tolerant metabolism and lack typical nutrient-scavenging mechanisms of free-living SRB. One trait, the glyoxylate bypass, was consistently expressed in situ and may serve both in reactive oxygen species defence and in biomass generation. The expression of oxygen-tolerant pathways, coupled with the loss of nutrient-scavenging functions, indicate specialization to a host-associated, redox-fluctuating environment distinct from that of free-living SRB. The symbiont genomes are also larger than those of free-living relatives, contrasting with genome reduction in many endosymbionts and reinforcing the importance of metabolic versatility. Our findings provide a framework for understanding how metabolic flexibility enables SRB to persist in long-term multipartite symbioses across diverse marine ecosystems.

Animal degradation of microbial storage polyhydroxyalkanoates.

A wide range of microorganisms produce storage biopolymer polyhydroxyalkanoates (sPHAs) as carbon and energy reserves. However, only bacteria and fungi are known to degrade microbial sPHAs, using enzymes called polyhydroxyalkanoate depolymerases (PHADs). Here we show that some animals also have PHADs that can degrade sPHAs. We discovered a PHAD in the gutless oligochaete Olavius algarvensis, a marine worm that gains nutrition by digesting bacterial symbionts, including a dominant symbiont in which sPHAs account for up to 42% of cellular carbon stores. Enzyme assays, combined with mass spectrometry, confirmed that heterologously expressed O. algarvensis PHAD degraded sPHAs into hydroxyalkanoate monomers that can enter conserved metabolic pathways. Imaging of mRNA showed that PHAD was expressed in the oligochaete epidermis, the site of symbiont digestion. We further identified PHADs in more than 66 gut-bearing animal species from nine phyla and 19 protist species from three major supergroups, suggesting that the last common ancestor of metazoans possessed PHADs. Functional assays confirmed that PHADs from phylogenetically distant animal lineages spanning aquatic and terrestrial environments degrade sPHAs. These findings reveal a previously unrecognized pathway by which protists and animals can access microbial carbon reserves, with broad relevance given the widespread occurrence of sPHAs across ecosystems.