Predominance of Cand. Patescibacteria in Groundwater Is Caused by Their Preferential Mobilization From Soils and Flourishing Under Oligotrophic Conditions

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 C...

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Main Authors: Martina Herrmann, Carl-Eric Wegner, Martin Taubert, Patricia Geesink, Katharina Lehmann, Lijuan Yan, Robert Lehmann, Kai Uwe Totsche, Kirsten Küsel
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.01407/full
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author Martina Herrmann
Martina Herrmann
Carl-Eric Wegner
Martin Taubert
Patricia Geesink
Katharina Lehmann
Lijuan Yan
Lijuan Yan
Robert Lehmann
Kai Uwe Totsche
Kirsten Küsel
Kirsten Küsel
author_facet Martina Herrmann
Martina Herrmann
Carl-Eric Wegner
Martin Taubert
Patricia Geesink
Katharina Lehmann
Lijuan Yan
Lijuan Yan
Robert Lehmann
Kai Uwe Totsche
Kirsten Küsel
Kirsten Küsel
author_sort Martina Herrmann
collection DOAJ
description 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.
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spelling doaj.art-7a2b0d9808e14195a38fe9072e3604802022-12-22T00:52:19ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-06-011010.3389/fmicb.2019.01407453214Predominance of Cand. Patescibacteria in Groundwater Is Caused by Their Preferential Mobilization From Soils and Flourishing Under Oligotrophic ConditionsMartina Herrmann0Martina Herrmann1Carl-Eric Wegner2Martin Taubert3Patricia Geesink4Katharina Lehmann5Lijuan Yan6Lijuan Yan7Robert Lehmann8Kai Uwe Totsche9Kirsten Küsel10Kirsten Küsel11Aquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University Jena, Jena, GermanyGerman Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, GermanyAquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University Jena, Jena, GermanyAquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University Jena, Jena, GermanyAquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University Jena, Jena, GermanyHydrogeology, Institute of Geosciences, Friedrich Schiller University Jena, Jena, GermanyAquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University Jena, Jena, GermanyGerman Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, GermanyHydrogeology, Institute of Geosciences, Friedrich Schiller University Jena, Jena, GermanyHydrogeology, Institute of Geosciences, Friedrich Schiller University Jena, Jena, GermanyAquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University Jena, Jena, GermanyGerman Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, GermanyDespite 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.https://www.frontiersin.org/article/10.3389/fmicb.2019.01407/fullshallow subsurfaceultra-small bacteriaoligotrophycommunity assemblyco-occurrenceCand. Patescibacteria
spellingShingle Martina Herrmann
Martina Herrmann
Carl-Eric Wegner
Martin Taubert
Patricia Geesink
Katharina Lehmann
Lijuan Yan
Lijuan Yan
Robert Lehmann
Kai Uwe Totsche
Kirsten Küsel
Kirsten Küsel
Predominance of Cand. Patescibacteria in Groundwater Is Caused by Their Preferential Mobilization From Soils and Flourishing Under Oligotrophic Conditions
Frontiers in Microbiology
shallow subsurface
ultra-small bacteria
oligotrophy
community assembly
co-occurrence
Cand. Patescibacteria
title Predominance of Cand. Patescibacteria in Groundwater Is Caused by Their Preferential Mobilization From Soils and Flourishing Under Oligotrophic Conditions
title_full Predominance of Cand. Patescibacteria in Groundwater Is Caused by Their Preferential Mobilization From Soils and Flourishing Under Oligotrophic Conditions
title_fullStr Predominance of Cand. Patescibacteria in Groundwater Is Caused by Their Preferential Mobilization From Soils and Flourishing Under Oligotrophic Conditions
title_full_unstemmed Predominance of Cand. Patescibacteria in Groundwater Is Caused by Their Preferential Mobilization From Soils and Flourishing Under Oligotrophic Conditions
title_short Predominance of Cand. Patescibacteria in Groundwater Is Caused by Their Preferential Mobilization From Soils and Flourishing Under Oligotrophic Conditions
title_sort predominance of cand patescibacteria in groundwater is caused by their preferential mobilization from soils and flourishing under oligotrophic conditions
topic shallow subsurface
ultra-small bacteria
oligotrophy
community assembly
co-occurrence
Cand. Patescibacteria
url https://www.frontiersin.org/article/10.3389/fmicb.2019.01407/full
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