Publications

3536

AbstractProtists frequently host diverse bacterial symbionts, in particular those affiliated with the order Holosporales (Alphaproteobacteria). All characterised members of this bacterial lineage have been retrieved in obligate association with a wide range of eukaryotes, especially multiple protist lineages (e.g. amoebozoans, ciliates, cercozoans, euglenids, and nucleariids), as well as some metazoans (especially arthropods and related ecdysozoans). While the genus Paramecium and other ciliates have been deeply investigated for the presence of symbionts, known members of the family “Candidatus Paracaedibacteraceae” (Holosporales) are currently underrepresented in such hosts. Herein, we report the description of “Candidatus Intestinibacterium parameciiphilum” within the family “Candidatus Paracaedibacteraceae”, inhabiting the cytoplasm of Paramecium biaurelia. This novel bacterium is almost twice as big as its relative “Candidatus Intestinibacterium nucleariae” from the opisthokont Nuclearia and does not present a surrounding halo. Based on phylogenetic analyses of 16S rRNA gene sequences, we identified six further potential species-level lineages within the genus. Based on the provenance of the respective samples, we investigated the environmental distribution of the representatives of “Candidatus Intestinibacterium” species. Obtained results are consistent with an obligate endosymbiotic lifestyle, with protists, in particular freshwater ones, as hosts. Thus, available data suggest that association with freshwater protists could be the ancestral condition for the members of the “Candidatus Intestinibacterium” genus.

Significance We report on cultivation and characterization of an association between Candidatus Nanohalobium constans and its host, the chitinotrophic haloarchaeon Halomicrobium LC1Hm, obtained from a crystallizer pond of marine solar salterns. High-quality nanohaloarchael genome sequence in conjunction with electron- and fluorescence microscopy, growth analysis, and proteomic and metabolomic data revealed mutually beneficial interactions between two archaea, and allowed dissection of the mechanisms for these interactions. Owing to their ubiquity in hypersaline environments, Nanohaloarchaeota may play a role in carbon turnover and ecosystem functioning, yet insights into the nature of this have been lacking. Here, we provide evidence that nanohaloarchaea can expand the range of available substrates for the haloarchaeon, suggesting that the ectosymbiont increases the metabolic capacity of the host.

AbstractThe Asgard superphylum is a deeply branching monophyletic group of Archaea, recently described as some of the closest relatives of the eukaryotic ancestor. The wide application of genomic analyses from metagenome sequencing has established six distinct phyla, whose genomes encode for diverse metabolic capacities and play important biogeochemical and ecological roles in marine sediments. Here, we describe two metagenome-assembled genomes (MAGs) recovered from deep marine sediments off Costa Rica margin, defining a novel lineage phylogenetically married to Thorarchaeota, as such we propose the name “Sifarchaeota” for this phylum. The two “Sifarchaeota” MAGs encode for an anaerobic methylotrophy pathway enabling the utilization of C1-C3 compounds (methanol and methylamines) to synthesize acetyl CoA. Also, the MAGs showed a remarkable saccharolytic capabilities compared to other Asgard lineages and encoded for diverse classes of carbohydrate active enzymes (CAZymes) targeting different mono-, di- and oligosaccharides. Comparative genomic analysis based on the full metabolic profiles of Asgard lineages revealed the close relation between “Sifarchaeota” and Odinarchaeota MAGs, which suggested a similar metabolic potentials and ecological roles. Furthermore, we identified multiple potential horizontal gene transfer (HGT) events from different bacterial donors within “Sifarchaetoa” MAGs, which hypothetically expanded “Sifarchaeota” capacities for substrate utilization, energy production and niche adaptation.ImportanceDeep marine sediments are the home of multiple poorly described archaeal lineages, many of which have ecological and evolutionary importance. We recovered metagenome-assembled genomes (MAGs) belonging to a novel Asgard phylum from the deep sediment of the Costa Rica margin. We proposed the name “Sifarchaeota” to describe the members of this phylum. Representative genomes of the “Sifarchaeota” showed remarkable saccharolytic capacities extending the known metabolic features encoded by the Asgard lineages. We attribute its ability to survive under the deep sediment conditions to its putative capacities to utilize different (C1-C3) compounds commonly encountered in deep sediment environments via anaerobic methylotrophy pathway. Also, we showed the importance of horizontal gene transfer in enhancing the “Sifarchaeota” collective adaptation strategies.

Anaerobic methane metabolism is among the hallmarks of Archaea, originating very early in their evolution. Here, we show that the ancestor of methane metabolizers was an autotrophic CO 2 -reducing hydrogenotrophic methanogen that possessed the two main complexes, methyl-CoM reductase (Mcr) and tetrahydromethanopterin-CoM methyltransferase (Mtr), the anaplerotic hydrogenases Eha and Ehb, and a set of other genes collectively called “methanogenesis markers” but could not oxidize alkanes. Overturning recent inferences, we demonstrate that methyl-dependent hydrogenotrophic methanogenesis has emerged multiple times independently, either due to a loss of Mtr while Mcr is inherited vertically or from an ancient lateral acquisition of Mcr. Even if Mcr is lost, Mtr, Eha, Ehb, and the markers can persist, resulting in mixotrophic metabolisms centered around the Wood-Ljungdahl pathway. Through their methanogenesis remnants, Thorarchaeia and two newly reconstructed order-level lineages in Archaeoglobi and Bathyarchaeia act as metabolically versatile players in carbon cycling of anoxic environments across the globe.

iaphorina citri is considered the most dangerous citrus pest because it transmits Candidatus Liberibacter asiaticus, the causal agent of Huanglongbing (HLB). Like other hemiptera insects, D. citri has developed mutualistic interactions with prokaryotic organisms known as endosymbionts. This symbiosis can be obligatory, when the interaction occurs with a primary endosymbiont, or facultative, when it is a secondary endosymbiont. Symbiosis is essential for various physiological functions, but some endosymbionts can adversely affect the psyllid's abilities. D. citri is associated with a great diversity of endosymbionts, with Candidatus Carsonella ruddii, Candidatus Profftella armatura, Candidatus Wolbachia spp. and Candidatus Liberibacter spp standing out. The aim o symbiotic relationship, prokaryotes, Candidatus Wolbachia, transmission of Candidatus Liberibacter asiaticus.

The recently described superphylum DPANN includes several phyla of uncultivated archaea with small cell sizes, reduced genomes, and limited metabolic capabilities. One of these phyla, “ Ca . Micrarchaeota,” comprises an enigmatic group of archaea found in acid mine drainage environments, the archaeal Richmond Mine acidophilic nanoorganisms (ARMAN) group. Analysis of their reduced genomes revealed the absence of key metabolic pathways consistent with their partner-associated lifestyle, and physical associations of ARMAN cells with their hosts were documented. However, “ Ca . Micrarchaeota” include several lineages besides the ARMAN group found in nonacidic environments, and none of them have been characterized. Here, we report a complete genome of “ Ca . Micrarchaeota” from a non-ARMAN lineage. Analysis of this genome revealed the presence of metabolic capacities lost in ARMAN genomes that could enable a free-living lifestyle. These results expand our understanding of genetic diversity, lifestyle, and evolution of “ Ca . Micrarchaeota.”