Simple Porifera holobiont reveals complex interactions between the host, an archaeon, a bacterium, and a phage.

The basal metazoan phylum, Porifera (sponges), is increasingly used as a model to investigate ecological and evolutionary features of microbe-animal symbioses. However, sponges often host complex microbiomes, which has hampered our understanding of their interactions with their microbial symbionts. Here, we describe the discovery and characterisation of the simplest sponge holobiont reported to date, consisting of the deep-sea glass sponge Aphrocalistes beatrix and two newly described microbial symbionts: an autotrophic ammonia-oxidising archaeon and a bacterial heterotroph. Omics analyses and metabolic modelling revealed the dependency of the ammonia-oxidising archaea on sponge-derived ammonia to drive primary production, which in turn supports the bacterium's growth by providing the dicarboxylate fumarate. Furthermore, virus-mediated archaeal lysis appears crucial to overcome the bacterium's vitamin B12 auxotrophy. These findings reveal that the exchange of vitamin B12 and dicarboxylate may be evolutionarily conserved features of symbiosis as they can also be found in interactions between free-living marine bacteria, and between microbes and plants or diatoms.

Bacteria associated with the in hospite Symbiodiniaceae's phycosphere.

Symbiotic interactions between Symbiodiniaceae and bacteria are still poorly explored, especially those in hospite. Here, we adapted a technique that allows for the enrichment of intact and metabolically active in hospite Symbiodiniaceae cells (ihSC) and their associated bacteria from the tissue of the model coral Pocillopora damicornis, using a discontinuous gradient of solution of isotonic Percoll (SIP). The ihSC were concentrated in the 50% SIP fraction, as determined by microscopy. The presence of bacteria associated with ihSC was confirmed by fluorescence in situ hybridization, while microbiome analysis indicated that bacteria of the families Halieaceae, Flavobacteriaceae, and Alcanivoraceae are significantly associated with ihSC. Extracellular vesicles that could be exuding molecules were detected on the symbiosome membranes. Our technique and data contribute to elucidate ihSC-bacteria interactions.

Species-specific relationships between deep sea sponges and their symbiotic Nitrosopumilaceae.

Sponges thrive in the deep, dark and nutrient-depleted ocean and may rely on microbial symbionts for carbon acquisition and energy generation. However, these symbiotic relationships remain largely unexplored. In this study, we analyze the microbiome of deep-sea sponges and show that ammonia-oxidizing archaea (AOA) of the family Nitrosopumilaceae make up at least 75% of the microbial communities of the sponges Aphrocallistes sp., Farrea sp. and Paratimea sp.. Given the known autotrophic metabolism of AOAs, this implies that these sponge holobionts can have the capacity for primary production in the deep-sea. We also show that specific AOA lineages are highly specific towards their hosts, hinting towards an unprecedent vertical transmission of these symbionts in deep-sea sponges. Our results show that the ecology and evolution of symbiotic relationships in deep-sea sponge is distinct from that of their shallow-water counterparts.

Carbon fixation pathways across the bacterial and archaeal tree of life.

Carbon fixation is a critical process for our planet; however, its distribution across the bacterial and archaeal domains of life has not been comprehensively studied. Here, we performed an analysis of 52,515 metagenome-assembled genomes and discover carbon fixation pathways in 1,007 bacteria and archaea. We reveal the genomic potential for carbon fixation through the reverse tricarboxylic acid cycle in previously unrecognized archaeal and bacterial phyla (i.e. Thermoplasmatota and Elusimicrobiota) and show that the 3-hydroxypropionate bi-cycle is not, as previously thought, restricted to the phylum Chloroflexota. The data also substantially expand the phylogenetic breadth for autotrophy through the dicarboxylate/4-hydroxybutyrate cycle and the Calvin-Benson-Bassham cycle. Finally, the genomic potential for carbon fixation through the 3-hydroxypropionate/4-hydroxybutyrate cycle, previously exclusively found in Archaea, was also detected in the Bacteria. Carbon fixation thus appears to be much more widespread than previously known, and this study lays the foundation to better understand the role of archaea and bacteria in global primary production and how they contribute to microbial carbon sinks.