Ecology, Evolution, Behavior and Systematics

Abstract Heritable symbionts are common in terrestrial arthropods and often provide beneficial services to hosts. Unlike obligate, nutritional symbionts that largely persist under strict host control within specialized host cells, heritable facultative symbionts exhibit large variation in within-host lifestyles and services rendered with many retaining the capacity to transition among roles. One enigmatic symbiont, Candidatus Fukatsuia symbiotica, frequently infects aphids with reported roles ranging from pathogen, defensive symbiont, mutualism exploiter and nutritional co-obligate symbiont. Here we used an in vitro culture-assisted protocol to sequence the genome of a facultative strain of Fukatsuia from pea aphids (Acyrthosiphon pisum). Phylogenetic and genomic comparisons indicate that Fukatsuia is an aerobic heterotroph, which together with Regiella insecticola and Hamiltonella defensa form a clade of heritable facultative symbionts within the Yersiniaceae (Enterobacteriales). These three heritable facultative symbionts largely share overlapping inventories of genes associated with housekeeping functions, metabolism, and nutrient acquisition, while varying in complements of mobile DNA. One unusual feature of Fukatsuia is its strong tendency to occur as a co-infection with H. defensa. However, the overall similarity of gene inventories among aphid heritable facultative symbionts suggest that metabolic complementarity is not the basis for co-infection, unless playing out on a H. defensa strain-specific basis. We also compared the pea aphid Fukatsuia with a strain from the aphid Cinara confinis (Lachninae) where it is reported to have transitioned to co-obligate status to support decaying Buchnera function. Overall the two genomes are very similar with no clear genomic signatures consistent with such a transition, which suggests co-obligate status in C. confinis was a recent event.

A novel actinomycete, designated strain GLM-1T, was isolated from arbuscular mycorrhizal fungal spores from Funneliformis mosseae RYA08, collected from Aquilaria crassna Pierre ex Lec. rhizosphere soil in Klaeng, Rayong Province, Thailand. Morphological characteristics of this strain included long chains of rod-like cells and squarish elements. The cell-wall composition of this novel isolate contained meso-diaminopimelic acid. The whole-cell diagnostic sugars were arabinose and galactose. The predominant menaquinone was MK-9(H4). The major fatty acids were iso-C16 : 0 and iso-C15 : 0. Only phosphatidylethanolamine was detected as a polar lipid. Phylogenetic analysis based on 16S rRNA gene sequences showed that strain GLM-1T was closely related to Amycolatopsis rhabdoformis SB026T (99.11 %) with a low DNA–DNA hybridization value of 22.6–34.7 %. Genome sequencing revealed a genome size of 10 Mbp. There were obvious distinctions in the average nucleotide identity values between stain GLM-1T and its closely related strains at around 86–93 % (ANIb) and 89–94 % (ANIm). The digital DNA–DNA hybridization values between strain GLM-1T and type strains of phylogenetically related species were 34–55 %. The G+C content of the genomic DNA was 71.8 mol%. Based on these data, strain GLM-1T is considered to represent a novel species of the genus Amycolatopsis , for which the name Amycolatopsis eburnea sp. nov. is proposed. The type strain is GLM-1T (=TBRC 9315T=NBRC 113658T)

Abstract The most abundant aquatic microbes are small in cell and genome size. Genome-streamlining theory predicts gene loss caused by evolutionary selection driven by environmental factors, favouring superior competitors for limiting resources. However, evolutionary histories of such abundant, genome-streamlined microbes remain largely unknown. Here we reconstruct the series of steps in the evolution of some of the most abundant genome-streamlined microbes in freshwaters (“Ca. Methylopumilus”) and oceans (marine lineage OM43). A broad genomic spectrum is visible in the family Methylophilaceae (Betaproteobacteria), from sediment microbes with medium-sized genomes (2–3 Mbp genome size), an occasionally blooming pelagic intermediate (1.7 Mbp), and the most reduced pelagic forms (1.3 Mbp). We show that a habitat transition from freshwater sediment to the relatively oligotrophic pelagial was accompanied by progressive gene loss and adaptive gains. Gene loss has mainly affected functions not necessarily required or advantageous in the pelagial or is encoded by redundant pathways. Likewise, we identified genes providing adaptations to oligotrophic conditions that have been transmitted horizontally from pelagic freshwater microbes. Remarkably, the secondary transition from the pelagial of lakes to the oceans required only slight modifications, i.e., adaptations to higher salinity, gained via horizontal gene transfer from indigenous microbes. Our study provides first genomic evidence of genome reduction taking place during habitat transitions. In this regard, the family Methylophilaceae is an exceptional model for tracing the evolutionary history of genome streamlining as such a collection of evolutionarily related microbes from different habitats is rare in the microbial world.

Abstract The actinobacterial acI lineage is among the most successful and ubiquitous freshwater bacterioplankton found on all continents, often representing more than half of all microbial cells in the lacustrine environment and constituting multiple ecotypes. However, stably growing pure cultures of the acI lineage have not been established despite various cultivation efforts based on ecological and genomic studies on the lineage, which is in contrast to the ocean from which abundant microorganisms such as Prochlorococcus, Pelagibacter, and Nitrosopumilus have been isolated. Here, we report the first two pure cultures of the acI lineage successfully maintained by supplementing the growth media with catalase. Catalase was critical for stabilizing the growth of acI strains irrespective of the genomic presence of the catalase-peroxidase (katG) gene. The two strains, representing two novel species, displayed differential phenotypes and distinct preferences for reduced sulfurs and carbohydrates, some of which were difficult to predict based on genomic information. Our results suggest that culture of previously uncultured freshwater bacteria can be facilitated by a simple catalase-supplement method and indicate that genome-based metabolic prediction can be complemented by physiological analyses.

Sponges represent ecologically important models to understand the evolution of symbiotic interactions of metazoans with microbial symbionts. Thaumarchaeota are commonly found in sponges, but their potential adaptations to a host-associated lifestyle are largely unknown. Here, we present three novel sponge-associated thaumarchaeal species and compare their genomic and predicted functional features with those of closely related free-living counterparts. We found different degrees of specialization of these thaumarchaeal species to the sponge environment that is reflected in their host distribution and their predicted molecular and metabolic properties. Our results indicate that Thaumarchaeota may have reached different stages of evolutionary adaptation in their symbiosis with sponges.

Summary Propionate is an important intermediate in the anaerobic mineralization of organic matter. In methanogenic environments, its degradation relies on syntrophic associations between syntrophic propionate‐oxidizing bacteria (SPOB) and Archaea . However, only 10 isolated species have been identified as SPOB so far. We report syntrophic propionate oxidation in thermophilic enrichments of Candidatus Syntrophosphaera thermopropionivorans, a novel representative of the candidate phylum Cloacimonetes . In enrichment culture, methane was produced from propionate, while Ca . S. thermopropionivorans contributed 63% to total bacterial cells. The draft genome of Ca . S. thermopropionivorans encodes genes for propionate oxidation via methymalonyl‐CoA. Phylogenetically, Ca . S. thermopropionivorans affiliates with the uncultured Cloacimonadaceae W5 and is more distantly related (86.4% 16S rRNA gene identity) to Ca . Cloacimonas acidaminovorans. Although Ca . S. thermopropionivorans was enriched from a thermophilic biogas reactor, Ca . Syntrophosphaera was in particular associated with mesophilic anaerobic digestion systems. 16S rRNA gene amplicon sequencng and a novel genus‐specific quantitative PCR assay consistently identified Ca . Syntrophosphaera/ Cloacimonadaceae W5 in 9 of 12 tested full‐scale biogas reactors thereby outnumbering other SPOB such as Pelotomaculum , Smithella and Syntrophobacter . Taken together the ubiquity and abundance of Ca . Syntrophosphaera, those SPOB might be key players for syntrophic propionate metabolism that have been overlooked before.

Abstract Several abundant but yet uncultivated bacterial groups exist in extreme iron- and sulfur-rich environments, and the physiology, biodiversity, and ecological roles of these bacteria remain a mystery. Here we retrieved four metagenome-assembled genomes (MAGs) from an artificial acid mine drainage (AMD) system, and propose they belong to a new deltaproteobacterial order, Candidatus Acidulodesulfobacterales. The distribution pattern of Ca. Acidulodesulfobacterales in AMDs across Southeast China correlated strongly with ferrous iron. Reconstructed metabolic pathways and gene expression profiles showed that they were likely facultatively anaerobic autotrophs capable of nitrogen fixation. In addition to dissimilatory sulfate reduction, encoded by dsrAB, dsrD, dsrL, and dsrEFH genes, these microorganisms might also oxidize sulfide, depending on oxygen concentration and/or oxidation reduction potential. Several genes with homology to those involved in iron metabolism were also identified, suggesting their potential role in iron cycling. In addition, the expression of abundant resistance genes revealed the mechanisms of adaptation and response to the extreme environmental stresses endured by these organisms in the AMD environment. These findings shed light on the distribution, diversity, and potential ecological role of the new order Ca. Acidulodesulfobacterales in nature.