Isolation and Genomics of Futiania mangrovii gen. nov., sp. nov., a Rare and Metabolically Versatile Member in the Class Alphaproteobacteria

Mangrove microorganisms are a major part of the coastal ecosystem and are directly associated with nutrient cycling. Despite their ecological significance, the collection of culturable mangrove microbes is limited due to difficulties in isolation and cultivation. Here, we report the isolation and genome sequence of strain FT118(T), the first cultured representative of a previously uncultivated order UBA8317 within Alphaproteobacteria, based on the combined results of 16S rRNA gene similarity, phylogenomic, and average amino acid identity analyses. We propose Futianiales ord. nov. and Futianiaceae fam. nov. with Futiania as the type genus, and FT118(T) represents the type species with the name Futiania mangrovii gen. nov, sp. nov. The 16S rRNA gene sequence comparison reveals that this novel order is a rare member but has a ubiquitous distribution across various habitats worldwide, which is corroborated by the experimental confirmation that this isolate can physiologically adapt to a wide range of oxygen levels, temperatures, pH and salinity levels. Biochemical characterization, genomic annotation, and metatranscriptomic analysis of FT118(T) demonstrate that it is metabolically versatile and active in situ. Genomic analysis reveals adaptive features of Futianiales to fluctuating mangrove environments, including the presence of high- and low-affinity terminal oxidases, N-type ATPase, and the genomic capability of producing various compatible solutes and polyhydroxybutyrate, which possibly allow for the persistence of this novel order across various habitats. Collectively, these results expand the current culture collection of mangrove microorganisms, providing genomic insights of how this novel taxon adapts to fluctuating environments and the culture reference to unravel possible microbe-environment interactions. IMPORTANCE The rare biosphere constitutes an essential part of the microbial community and may drive nutrient cycling and other geochemical processes. However, the difficulty in microbial isolation and cultivation has hampered our understanding of the physiology and ecology of uncultured rare lineages. In this study, we successfully isolated a novel alphaproteobacterium, designated as FT118(T), and performed a combination of phenotypic, phylogenetic, and phylogenomic analyses, confirming that this isolate represents the first cultured member of a previously uncultivated order UBA8317 within Alphaproteobacteria. It is a rare species with a ubiquitous distribution across different habitats. Genomic and metatranscriptomic analyses demonstrate that it is metabolically versatile and active in situ, suggesting its potential role in nutrient cycling despite being scarce. This work not only expands the current phylogeny of isolated Alphaproteobacteria but also provides genomic and culture reference to unravel microbial adaptation strategies in mangrove sediments and possible microbe-environment interactions.