It is revealed that a globally distributed clade of symbiotic SRB has a conserved core metabolism that diverges from free-living relatives, and 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.
Abstract
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.
Marine sponges associate with microbial symbionts that shape host physiology and drive nutrient cycling, yet assigning partner-specific contributions to holobiont metabolism remains challenging in species with complex microbiomes. The coral reef demosponge Amphimedon queenslandica offers tractable resolution, as its adult microbiome is dominated by just three extracellular, vertically inherited gammaproteobacterial symbionts (AqS1, AqS2 and AqS3). Here, we present improve genome assemblies of the host and each symbiont, integrated with adult holotranscriptomes to resolve functional partitioning and expressed pathway capacity of each partner. Despite representing only ∼20% of KEGG-annotated hologenome genes, the three symbionts contribute 45.2 and 72% of metabolic and membrane transporter genes, respectively, revealing a pronounced functional imbalance in proteins involved in nutrient transformation and exchange. Although central heterotrophic carbon metabolism is complete across all four partners, gene content and expression are consistent with symbiont uptake of host-liberated carbohydrates. Complementation of pathways occurs across dissolved inorganic nutrient assimilation, including nitrate reduction, sulfur redox metabolism, and phosphate uptake and storage. Symbionts further expand holobiont biosynthetic breadth through amino acid, vitamin, and co-factor pathways that are incomplete or absent from the host, coupled with expressed membrane transporter repertoires consistent with directed metabolite exchange. Together, these results show that vertically inherited symbionts can disproportionately expand holobiont metabolic capacity, with membrane transporter enrichment linking symbiont metabolic breadth to host physiology. This exchange-oriented functional architecture, rather than simple pathway redundancy, appears to underlie metabolic integration in this low-complexity animal– microbe symbiosis.
Xueyan Xiang, E. Maunders, B. Degnan et al.· bioRxiv· 0 citations
Blood-feeding insects typically depend on obligate intracellular bacterial symbionts that provide essential B vitamins absent from vertebrate blood. In contrast, kissing bugs (Triatominae) have long been considered atypical because they rely primarily on extracellular gut-associated bacteria. Recent reports of the genus Symbiopectobacterium in Rhodnius species raise questions about the diversity and evolution of symbiosis in these insects. Here, we investigate the distribution, genome evolution, and tissue localization of Symbiopectobacterium in the genus Rhodnius. Using comparative metagenomics, phylogenomics, fluorescence in situ hybridization, transmission electron microscopy, and hemolymph screening, we characterize a Symbiopectobacterium genome from Rhodnius prolixus and assess its occurrence across publicly available datasets representing multiple Rhodnius species. The R. prolixus strain possesses a large, highly dynamic genome enriched in mobile genetic elements, pseudogenes, and remnants of secretion systems, while retaining biosynthetic pathways for several B vitamins. Comparative analysis revealed variation in genome reduction among Rhodnius-associated strains, suggesting ongoing and potentially independent transitions toward host-restricted symbiosis. Localization analyses detected Symbiopectobacterium intracellularly within posterior midgut epithelial cells and occasionally in the hemolymph, consistent with a facultative intracellular lifestyle. However, no bacteriomes or stable intracellular structures were observed. Together, these findings indicate that Symbiopectobacterium represents an intermediate stage in the transition from environmentally associated bacteria to obligate intracellular mutualists in Triatominae.
Tanisha Moons, S. Mendiola, Hassan Tarabai et al.· bioRxiv· 0 citations
Sulfate-reducing microbiomes (SRMs) have shown strong potential for antibiotic remediation, yet the active microorganisms and community-level strategies associated with sulfamethoxazole (SMX) biotransformation remain poorly understood. In this study, long-term bioreactor operation (269 days; 500-1500 μg/L SMX), DNA-stable isotope probing (DNA-SIP), and metagenomic analyses were integrated to investigate the microbial contributors and functional organization underlying SRM-driven SMX biotransformation. Desulfobacterium, a key SRM member, was co-enriched with Geobacter and Leptolinea in the 13C-labeled heavy fraction, suggesting potential metabolic complementarity during community-level SMX biotransformation. Genome-resolved analyses further revealed structured patterns of inferred horizontal gene transfer (HGT) and predicted metabolite exchange among keystone taxa. The transferred genes were mainly associated with energy conservation, transport, sulfur-associated metabolism, and stress-response functions, whereas the predicted exchanged metabolites included carbon metabolites, amino acid-related sulfur compounds, purine-related intermediates, and cofactor-associated metabolites. Together, these findings suggest that HGT-associated functional redistribution and metabolic complementarity may contribute to the persistence and coordinated activity of sulfate-reducing microbiomes under high SMX stress. This study links SIP-identified active populations with genome-inferred interaction patterns in a sulfate-reducing system and provides new insight into microbiome-based anaerobic strategies for antibiotic-containing wastewater treatment.
Yanyan Jia, Yujian Yan, Ben Chen et al.· Environmental Science and Te...· 0 citations
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.
Caroline Zeidler, Harald R Gruber-Vodicka, D. Michellod et al.· Nature Ecology & Evolution· 0 citations
