Abstract
Acidobacteria occur in a large variety of ecosystems worldwide and are particularly abundant and highly diverse in soils. In spite of their diversity, only few species have been characterized to date which makes Acidobacteria one of the most poorly understood phyla among the domain Bacteria. We used a culture-independent niche modeling approach to elucidate ecological adaptations and their evolution for 4,154 operational taxonomic units (OTUs) of Acidobacteria across 150 different, comprehensively characterized grassland soils in Germany. Using the relative abundances of their 16S rRNA gene transcripts, the responses of active OTUs along gradients of 41 environmental variables were modeled using hierarchical logistic regression (HOF), which allowed to determine values for optimum activity for each variable (niche optima). By linking 16S rRNA transcripts to the phylogeny of full 16S rRNA gene sequences, we could trace the evolution of the different ecological adaptations during the diversification of Acidobacteria. This approach revealed a pronounced ecological diversification even among acidobacterial sister clades. Although the evolution of habitat adaptation was mainly cladogenic, it was disrupted by recurrent events of convergent evolution that resulted in frequent habitat switching within individual clades. Our findings indicate that the high diversity of soil acidobacterial communities is largely sustained by differential habitat adaptation even at the level of closely related species. A comparison of niche optima of individual OTUs with the phenotypic properties of their cultivated representatives showed that our niche modeling approach (1) correctly predicts those physiological properties that have been determined for cultivated species of Acidobacteria but (2) also provides ample information on ecological adaptations that cannot be inferred from standard taxonomic descriptions of bacterial isolates. These novel information on specific adaptations of not-yet-cultivated Acidobacteria can therefore guide future cultivation trials and likely will increase their cultivation success.
Highlights
Acidobacteria occur globally in a wide variety of ecosystems
phylogenetic eigenvector regression (PVR) starts by extracting eigenvectors [using a principal coordinate analysis (PCoA)] from pairwise distance matrices that describe the phylogenetic relationships among species and use some of the eigenvectors to model trait variation with a standard ordinary least-squares (OLS) regression
The acidobacterial reads were assigned to a backbone phylogenetic tree of full-length 16S rRNA genes sequences constructed for 5,450 reference OTUs using a 99% identity cutoff, which made it possible to compute the relative abundances of 16S RNA gene transcripts for the different Acidobacteria OTUs in the different soil samples
Summary
Acidobacteria occur globally in a wide variety of ecosystems. The phylum encompasses a phylogenetically broad diversity of bacteria that were initially assigned to 26 subdivisions (SDs; Barns et al, 2007) and more recently into 15 classes (Dedysh and Yilmaz, 2018). Of the acidobacterial 16S rRNA gene sequences that have associated meta-data, 54.9% originate from soils and 20.3% from (semi-)aquatic sediments. In contrast to their high abundance and diversity, only 61 validly named species from 27 genera (in addition to two Candidatus genera with one species each) could be described to date. Discrepancies between genomic predictions and physiological activities have frequently been observed (Kielak et al, 2016a; Rodrigues et al, 2020) Aside from these few known functions, the ecologically relevant traits of the majority of Acidobacteria species have remained mostly unknown. For a subset of these grassland soils, a previous study had provided evidence for an adaptation of individual acidobacterial species to specific environmental factors (Naether et al, 2012; Foesel et al, 2014)
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