Abstract
Despite the widely observed predominance of Cand. Patescibacteria in subsurface communities, their input source and ecophysiology are poorly understood. Here we study mechanisms of the formation of a groundwater microbiome and the subsequent differentiation of Cand. Patescibacteria. In the Hainich Critical Zone Exploratory, Germany, we trace the input of microorganisms from forested soils of preferential recharge areas through fractured aquifers along a 5.4 km hillslope well transect. Cand. Patescibacteria were preferentially mobilized from soils and constituted 66% of species-level OTUs shared between seepage and shallow groundwater. These OTUs, mostly related to Cand. Kaiserbacteraceae, Cand. Nomurabacteraceae, and unclassified UBA9983 at the family level, represented a relative abundance of 71.4% of the Cand. Patescibacteria community at the shallowest groundwater well, and still 44.4% at the end of the transect. Several Cand. Patescibacteria subclass-level groups exhibited preferences for different conditions in the two aquifer assemblages investigated: Cand. Kaiserbacteraceae surprisingly showed positive correlations with oxygen concentrations, while Cand. Nomurabacteraceae were negatively correlated. Co-occurrence network analysis revealed a central role of Cand. Patescibacteria in the groundwater microbial communities and pointed to potential associations with specific organisms, including abundant autotrophic taxa involved in nitrogen, sulfur and iron cycling. Strong associations among Cand. Patescibacteria themselves further suggested that for many groups within this phylum, distribution was mainly driven by conditions commonly supporting a fermentative life style without direct dependence on specific hosts. We propose that import from soil, and community differentiation driven by hydrochemical conditions, including the availability of organic resources and potential hosts, determine the success of Cand. Patescibacteria in groundwater environments.
Highlights
In recent years, the bacterial tree of life underwent a tremendous expansion through the discovery of the immense microbial diversity within the ‘candidate phyla radiation’ (CPR) (Hug et al, 2016)
Patescibacteria represented the largest fraction of the groundwater microbial communities, with relative abundances ranging from 17 to 79%
Patescibacteria were especially enriched in the ultra-small fraction of cells: Following sequential filtration of groundwater through 0.2 and 0.1 μm pore size filters, up to 83% of the community collected on the 0.1 μm pore size filters were related to class Cand
Summary
The bacterial tree of life underwent a tremendous expansion through the discovery of the immense microbial diversity within the ‘candidate phyla radiation’ (CPR) (Hug et al, 2016). Recent phylogenetic and taxonomic analyses suggested the reclassification of the CPR as a single phylum, Cand. Patescibacteria (Parks et al, 2018), with 14 classes known so far. The majority of these taxa were predicted based on metagenomic analysis of habitats difficult to access, such as groundwater, deep sea sediments, permafrost, and the continental deep subsurface (Brown et al, 2015; Luef et al, 2015; Frey et al, 2016; Hubalek et al, 2016; Léon-Zayas et al, 2017). As available information about these organisms is derived almost exclusively from (meta)genomic analyses, research needs to be aimed at elucidating their origin and ecophysiology to understand their success in these habitats
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