Spatial Variability in Streambed Microbial Community Structure across Two Watersheds

ABSTRACT Both spatial and temporal variability are key attributes of sedimentary microbial communities, and while spatial effects on beta-diversity appear to dominate at larger distances, the character of spatial variability at finer scales remains poorly understood, especially for headwater stream...

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Main Authors: Philips O. Akinwole, Jinjun Kan, Louis A. Kaplan, Robert H. Findlay
Format: Article
Language:English
Published: American Society for Microbiology 2021-12-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/Spectrum.01972-21
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author Philips O. Akinwole
Jinjun Kan
Louis A. Kaplan
Robert H. Findlay
author_facet Philips O. Akinwole
Jinjun Kan
Louis A. Kaplan
Robert H. Findlay
author_sort Philips O. Akinwole
collection DOAJ
description ABSTRACT Both spatial and temporal variability are key attributes of sedimentary microbial communities, and while spatial effects on beta-diversity appear to dominate at larger distances, the character of spatial variability at finer scales remains poorly understood, especially for headwater stream communities. We investigated patterns of microbial community structure (MCS) in biofilms attached to streambed sediments from two watersheds across spatial scales spanning <1 m within a single stream to several hundred kilometers between watersheds. Analyses of phospholipid fatty acid (PLFA) profiles indicated that the variations in MCS were driven by increases in the relative abundance of microeukaryotic photoautotrophs and their contribution to total microbial biomass. Furthermore, streams within watersheds had similar MCS, underscoring watershed-level controls of microbial communities. Moreover, bacterial community structure assayed as either PCR-denaturing gradient gel electrophoresis (PCR-DGGE) fingerprints or PLFA profiles edited to remove microeukaryotes indicated a distinct watershed-level biogeography. No distinct stream order-level distributions were identified, although DGGE analyses clearly indicated that there was greater variability in community structure among 1st-order streams than among 2nd- and 3rd-order streams. Longitudinal gradients in microbial biomass and structure showed that the greatest variations were associated with 1st-order streams within a watershed, and 68% of the variation in total microbial biomass was explained by sediment atomic carbon-to-nitrogen ratio (C:N ratio), percent carbon, sediment surface area, and percent water content. This study confirms a distinct microbial biogeography for headwater stream communities driven by environmental heterogeneity across distant watersheds and suggests that eukaryotic photoautotrophs play a key role in structuring bacterial communities on streambed sediments. IMPORTANCE Microorganisms in streams drive many biogeochemical reactions of global significance, including nutrient cycling and energy flow; yet, the mechanisms responsible for the distribution and composition of streambed microbial communities are not well known. We sampled sediments from multiple streams in two watersheds (Neversink River [New York] and White Clay Creek [WCC; Pennsylvania] watersheds) and measured microbial biomass and total microbial and bacterial community structures using phospholipid and molecular methods. Microbial and bacterial community structures displayed a distinct watershed-level biogeography. The smallest headwater streams within a watershed showed the greatest variation in microbial biomass, and 68% of that variation was explained by the atomic carbon-to-nitrogen ratio (C:N ratio), percent carbon, sediment surface area, and percent water content. Our study revealed a nonrandom distribution of microbial communities in streambeds, and showed that microeukaryotic photoautotrophs, environmental heterogeneity, and geographical distance influence microbial composition and spatial distribution.
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spelling doaj.art-65f3d0527001426799ee65fe965394d52022-12-22T04:15:51ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972021-12-019310.1128/Spectrum.01972-21Spatial Variability in Streambed Microbial Community Structure across Two WatershedsPhilips O. Akinwole0Jinjun Kan1Louis A. Kaplan2Robert H. Findlay3Biology Department, DePauw University, Greencastle, Indiana, USAStroud Water Research Center, Avondale, Pennsylvania, USAStroud Water Research Center, Avondale, Pennsylvania, USADepartment of Biological Sciences, University of Alabama, Tuscaloosa, Alabama, USAABSTRACT Both spatial and temporal variability are key attributes of sedimentary microbial communities, and while spatial effects on beta-diversity appear to dominate at larger distances, the character of spatial variability at finer scales remains poorly understood, especially for headwater stream communities. We investigated patterns of microbial community structure (MCS) in biofilms attached to streambed sediments from two watersheds across spatial scales spanning <1 m within a single stream to several hundred kilometers between watersheds. Analyses of phospholipid fatty acid (PLFA) profiles indicated that the variations in MCS were driven by increases in the relative abundance of microeukaryotic photoautotrophs and their contribution to total microbial biomass. Furthermore, streams within watersheds had similar MCS, underscoring watershed-level controls of microbial communities. Moreover, bacterial community structure assayed as either PCR-denaturing gradient gel electrophoresis (PCR-DGGE) fingerprints or PLFA profiles edited to remove microeukaryotes indicated a distinct watershed-level biogeography. No distinct stream order-level distributions were identified, although DGGE analyses clearly indicated that there was greater variability in community structure among 1st-order streams than among 2nd- and 3rd-order streams. Longitudinal gradients in microbial biomass and structure showed that the greatest variations were associated with 1st-order streams within a watershed, and 68% of the variation in total microbial biomass was explained by sediment atomic carbon-to-nitrogen ratio (C:N ratio), percent carbon, sediment surface area, and percent water content. This study confirms a distinct microbial biogeography for headwater stream communities driven by environmental heterogeneity across distant watersheds and suggests that eukaryotic photoautotrophs play a key role in structuring bacterial communities on streambed sediments. IMPORTANCE Microorganisms in streams drive many biogeochemical reactions of global significance, including nutrient cycling and energy flow; yet, the mechanisms responsible for the distribution and composition of streambed microbial communities are not well known. We sampled sediments from multiple streams in two watersheds (Neversink River [New York] and White Clay Creek [WCC; Pennsylvania] watersheds) and measured microbial biomass and total microbial and bacterial community structures using phospholipid and molecular methods. Microbial and bacterial community structures displayed a distinct watershed-level biogeography. The smallest headwater streams within a watershed showed the greatest variation in microbial biomass, and 68% of that variation was explained by the atomic carbon-to-nitrogen ratio (C:N ratio), percent carbon, sediment surface area, and percent water content. Our study revealed a nonrandom distribution of microbial communities in streambeds, and showed that microeukaryotic photoautotrophs, environmental heterogeneity, and geographical distance influence microbial composition and spatial distribution.https://journals.asm.org/doi/10.1128/Spectrum.01972-21microbial community structuremicrobial biomassmicrobial biogeographymicroeukaryotesPLFADGGE
spellingShingle Philips O. Akinwole
Jinjun Kan
Louis A. Kaplan
Robert H. Findlay
Spatial Variability in Streambed Microbial Community Structure across Two Watersheds
Microbiology Spectrum
microbial community structure
microbial biomass
microbial biogeography
microeukaryotes
PLFA
DGGE
title Spatial Variability in Streambed Microbial Community Structure across Two Watersheds
title_full Spatial Variability in Streambed Microbial Community Structure across Two Watersheds
title_fullStr Spatial Variability in Streambed Microbial Community Structure across Two Watersheds
title_full_unstemmed Spatial Variability in Streambed Microbial Community Structure across Two Watersheds
title_short Spatial Variability in Streambed Microbial Community Structure across Two Watersheds
title_sort spatial variability in streambed microbial community structure across two watersheds
topic microbial community structure
microbial biomass
microbial biogeography
microeukaryotes
PLFA
DGGE
url https://journals.asm.org/doi/10.1128/Spectrum.01972-21
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AT jinjunkan spatialvariabilityinstreambedmicrobialcommunitystructureacrosstwowatersheds
AT louisakaplan spatialvariabilityinstreambedmicrobialcommunitystructureacrosstwowatersheds
AT roberthfindlay spatialvariabilityinstreambedmicrobialcommunitystructureacrosstwowatersheds