Microdiversification in genome-streamlined ubiquitous freshwater Actinobacteria

Abstract

Actinobacteria of the acI lineage are the most abundant microbes in freshwater systems, but there are so far no pure living cultures of these organisms, possibly because of metabolic dependencies on other microbes. This, in turn, has hampered an in-depth assessment of the genomic basis for their success in the environment. Here we present genomes from 16 axenic cultures of acI Actinobacteria. The isolates were not only of minute cell size, but also among the most streamlined free-living microbes, with extremely small genome sizes (1.2-1.4 Mbp) and low genomic GC content. Genome reduction in these bacteria might have led to auxotrophy for various vitamins, amino acids and reduced sulphur sources, thus creating dependencies to co-occurring organisms (the 'Black Queen' hypothesis). Genome analyses, moreover, revealed a surprising degree of inter-and intraspecific diversity in metabolic pathways, especially of carbohydrate transport and metabolism, and mainly encoded in genomic islands. The striking genotype microdiversification of acI Actinobacteria might explain their global success in highly dynamic freshwater environments with complex seasonal patterns of allochthonous and autochthonous carbon sources. We propose a new order within Actinobacteria ('Candidatus Nanopelagicales') with two new genera ('Candidatus Nanopelagicus' and 'Candidatus Planktophila') and nine new species. DOI: https://doi.org/10. 1038/ismej.2017.156 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-144935 Journal Article Accepted Version Originally published at: Neuenschwander, Stefan M; Ghai, Rohit; Pernthaler, Jakob; Salcher, Michaela M (2018). Microdiversification in genome-streamlined ubiquitous freshwater Actinobacteria. The ISME journal,

Geomicrobiology of the carbon, nitrogen and sulphur cycles in Powell Lake: a permanently stratified water column containing ancient seawater

“…SAR11 is highly abundant in the oxygenated surface ocean and also in mOMZs (Wright et al ., ; Bertagnolli and Stewart, ). Similarities based on small genome and cell sizes between acI and SAR11 have been noted previously (Neuenschwander et al ., ). Here we find indications that acI lineages in meromictic Powell Lake, like SAR11 lineages from mOMZs (Tsementzi et al ., ), stand out from their strictly aerobic relatives by facultative anaerobic adaptations, notably the possession of genes for respiratory nitrate reduction.…”

“…In Powell Lake, an OTU affiliated with acI dominated the oxycline and nitrogenous zones and remained prevalent even in the manganous zone (Table 1). Its closest neighbour (99% sequence identity, blastN) was Candidatus 'Planktophila vernalis' isolate MMS-IIA-15 (NZ_CP016776.1; Neuenschwander et al, 2018). The high relative abundance of acI within and below the oxycline may be due to undocumented facultative anaerobic adaptations in Powell Lake strains (Ghylin et al, 2014).…”

Microbial life under ice: Metagenome diversity and in situ activity of Verrucomicrobia in seasonally ice‐covered Lakes

“…Ice-covered conditions may favour microbes that have low resource requirements (i.e., oligotrophs) and small genome size is a common adaptation to oligotrophic conditions (Carini et al, 2013;Neuenschwander et al, 2017). Previous analysis of Verrucomicrobia MAGs have shown a wide range in genome sizes (Cabello-Yeves et al, 2017a).…”

Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake

“…Whereas nearly identical viral genomes have been reported from distant locations in marine environments, such as the Mediterranean Sea and Pacific Ocean , these results in freshwater systems are intriguing, as lakes and reservoirs are physically isolated from one another. By contrast, the genomes of their host (i.e., bacterioplankton) inhabiting different freshwater systems are generally distinct (Hahn et al, 2016;Kang et al, 2017;Garcia et al, 2018;Neuenschwander et al, 2018), although highly similar genomes (ANI >95%) have occasionally been reported from lakes on different continents (Mehrshad et al, 2018). The high phylogeographic connectivity of viruses was presumably because viruses can easily colonize a new habitat due to the lack of immunity by local hosts, whereas colonization by bacteria is often constrained by the priority effect, that is, occupation of the niche by prior inhabitants limits settlement of newly migrated genotypes (Incagnone et al, 2015).…”