skip to main content

This content will become publicly available on April 28, 2025

Title: Porewater microbiomes in buried wetland soils: Synergic effects of water chemistry and redox gradients associated with hydrological processes

Interstitial water or pore water occupies the space between soil particles and provides “hotspots” and “fluvial networks” for microbial activities in floodplain soil. However, to date, we know very little about the microorganisms living in pore water and how they respond to environmental changes. This study aimed to understand microbial distribution and assemblage in riparian pore waters, and how they respond to water chemistry and redox gradients associated with hydrological processes.

We analysed the annual changes of porewater microbial communities from the east and west banks of the White Clay Creek, a site at the Christina River Basin – Critical Zone Observatory, Pennsylvania, USA. Microbial abundances were quantified by epifluorescence microscopy and detailed community structures were characterised by high‐throughput sequencing. Water chemistry and redox gradients were also monitored and recorded, and their interactions with porewater microbiomes were analysed using correlations and multivariate analyses.

Abundance of microbial cells increased during summer and late autumn. Wetland porewater microbiomes mainly contained Acidobacteria, Bacteroidetes, Nitrospirae and Proteobacteria, and microbiome structures were easily distinguishable from those in the underlying hyporheic gravel layer. Seasonal dynamics of bacterial community structure in the east and west wetlands were distinct, responding to floodplain topography and associated hydrological/geochemical processes. Iron (Fe)‐cycling bacteria (mainly Gallionellaceae andRhodoferaxspp.) dominated the porewater microbiome, and their relative abundance was significantly higher in the east than the west wetland. Furthermore, Fe‐oxidising bacteria (Gallionellaceae) were negatively correlated with Fe‐reducing bacteria (Rhodoferaxspp.) at the east wetland.

Microbial abundances (cell density) in pore waters showed similar seasonal patterns across stream banks, but microbial community structure did not. Microbiome assembly in pore water is correlated with water chemistry and redox gradients primarily associated with local hydrological processes.

As a consequence of their significance for carbon (C) mineralisation and Fe reduction at terrestrial–aquatic interfaces, microbiomes in riparian pore waters and associated microbial activity play an essential role in C and mineral dynamics. These findings will inform future studies of the response of freshwater ecosystems to hydrological dynamics influenced by global climate change.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
Freshwater Biology
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Freshwater mussels are important for nutrient cycling and ecosystem health as they filter feed on their surrounding water. This filter feeding makes these bivalves especially sensitive to conditions in their environment. Gut microbial communities (microbiomes) have been recognised as important to both host organism and ecosystem health; however, how freshwater mussel microbiomes are organised and influenced is unclear.

    In this study, the gut bacterial microbiome of Threeridge mussel,Amblema plicata, was compared across two river basins, five rivers, and nine local sites in the south‐eastern U.S.A. Mussel gut tissue was dissected, DNA extracted, and the microbiome characterised by high throughput sequencing of the V4 region of the 16S ribosomal RNA gene.

    Planctomycetes, Firmicutes, and Cyanobacteria were the most common bacterial phyla within the guts of all sampledA.plicata. However, the relative abundances of these major bacterial phyla differed between mussels sampled from different rivers and river basins, as did the relative abundance of specific bacterial operational taxonomic units (OTUs). Despite these differences, a core microbiome was identified across all mussels, with eight OTUs being consistent members of theA.plicatamicrobiome at all sites, the most abundant OTU identifying as a member of the family Planctomycetaceae. Geographic distance between sites was not correlated with similarity in the structure of the gut microbiome, which was more related to site physicochemistry.

    Overall, these results suggest that while physicochemical conditions affect the composition of transient bacteria in the Threeridge mussel gut microbiome, the core microbiome is largely unaffected, and a portion of theA.plicatamicrobiome is retained regardless of the river system.

    How long transient bacteria remain in the gut, and to what extent these transient microbes aid in host function is still unknown. Core microbiota have been found to aid in multiple functions within animal hosts, and within freshwater mussels this core microbiome may aid in nutrient processing and cycling. Therefore, it is important to look at both transient and core microbes when studying the structure of freshwater invertebrate microbiomes.

    more » « less
  2. Summary

    Habitat fragmentation is a leading cause of biodiversity and ecosystem function loss in the Anthropocene. Despite the importance of plant–microbiome interactions to ecosystem productivity, we have limited knowledge of how fragmentation affects microbiomes and even less knowledge of its consequences for microbial interactions with plants.

    Combining field surveys, microbiome sequencing, manipulative experiments, and random forest models, we investigated fragmentation legacy effects on soil microbiomes in imperiled pine rocklands, tested how compositional shifts across 14 fragmentation‐altered soil microbiomes affected performance and resource allocation of three native plant species, and identified fragmentation‐responding microbial families underpinning plant performance.

    Legacies of habitat fragmentation were associated with significant changes in microbial diversity and composition (across three of four community axes). Experiments showed plants often strongly benefited from the microbiome’s presence, but fragmentation‐associated changes in microbiome composition also significantly affected plant performance and resource allocation across all seven metrics examined. Finally, random forest models identified ten fungal and six bacterial families important for plant performance that changed significantly with fragmentation.

    Our findings not only support the existence of significant fragmentation effects on natural microbiomes, but also demonstrate for the first time that fragmentation‐associated changes in microbiomes can have meaningful consequences for native plant performance and investment.

    more » « less
  3. Summary

    Allelopathy is a common and important stressor that shapes plant communities and can alter soil microbiomes, yet little is known about the direct effects of allelochemical addition on bacterial and fungal communities or the potential for allelochemical‐selected microbiomes to mediate plant performance responses, especially in habitats naturally structured by allelopathy.

    Here, we present the first community‐wide investigation of microbial mediation of allelochemical effects on plant performance by testing how allelopathy affects soil microbiome structure and how these microbial changes impact germination and productivity across 13 plant species.

    The soil microbiome exhibited significant changes to ‘core’ bacterial and fungal taxa, bacterial composition, abundance of functionally important bacterial and fungal taxa, and predicted bacterial functional genes after the addition of the dominant allelochemical native to this habitat. Furthermore, plant performance was mediated by the allelochemical‐selected microbiome, with allelopathic inhibition of plant productivity moderately mitigated by the microbiome.

    Through our findings, we present a potential framework to understand the strength of plant–microbial interactions in the presence of environmental stressors, in which frequency of the ecological stress may be a key predictor of microbiome‐mediation strength.

    more » « less
  4. Abstract

    Although stability is relatively well understood in macro‐organisms, much less is known about its drivers in host–microbial systems where processes operating at multiple levels of biological organisation jointly regulate the microbiome.

    We conducted an experiment to examine the microbiome stability of three Caribbean corals (Acropora cervicornis,Pseudodiploria strigosaandPorites astreoides) by placing them in aquaria and exposing them to a pulse perturbation consisting of a large dose of broad‐spectrum antibiotics before transplanting them into the field.

    We found that coral hosts harboured persistent, species‐specific microbiomes. Stability was generally high but variable across coral species, withA. cervicornismicrobiomes displaying the lowest community turnover in both the non‐perturbed and the perturbed field transplants. Interestingly, the microbiome ofP. astreoideswas stable in the non‐perturbed field transplants, but unstable in the perturbed field transplants.

    A mathematical model of host–microbial dynamics helped resolve this paradox by showing that when microbiome regulation is driven by host sanctioning, both resistance and resilience to invasion are low and can lead to instability despite the high direct costs bourne by corals. Conversely, when microbiome regulation is mainly associated with microbial processes, both resistance and resilience to invasion are high and promote stability at no direct cost to corals. We suggest that corals that are mainly regulated by microbial processes can be likened to ‘glass cannons’ because the high stability they exhibit in the field is due to their microbiome's potent suppression of invasive microbes. However, these corals are susceptible to destabilisation when exposed to perturbations that target the vulnerable members of their microbiomes who are responsible for mounting such powerful attacks against invasive microbes. The differential patterns of stability exhibited byP. astreoidesacross perturbed and non‐perturbed field transplants suggest it is a ‘glass cannon’ whose microbiome is regulated by microbial processes, whereasA. cervicornis’ consistent patterns of stability suggest that its microbiome is mainly regulated by host‐level processes.

    Our results show that understanding how processes that operate at multiple levels of biological organisation interact to regulate microbiomes is critical for predicting the effects of environmental perturbations on host–microbial systems.

    more » « less
  5. Summary

    Macroorganisms’ genotypes shape their phenotypes, which in turn shape the habitat available to potential microbial symbionts. This influence of host genotype on microbiome composition has been demonstrated in many systems; however, most previous studies have either compared unrelated genotypes or delved into molecular mechanisms. As a result, it is currently unclear whether the heritability of host‐associated microbiomes follows similar patterns to the heritability of other complex traits.

    We take a new approach to this question by comparing the microbiomes of diverse maize inbred lines and their F1hybrid offspring, which we quantified in both rhizosphere and leaves of field‐grown plants using 16S‐v4 and ITS1 amplicon sequencing.

    We show that inbred lines and hybrids differ consistently in the composition of bacterial and fungal rhizosphere communities, as well as leaf‐associated fungal communities. A wide range of microbiome features display heterosis within individual crosses, consistent with patterns for nonmicrobial maize phenotypes. For leaf microbiomes, these results were supported by the observation that broad‐sense heritability in hybrids was substantially higher than narrow‐sense heritability.

    Our results support our hypothesis that at least some heterotic host traits affect microbiome composition in maize.

    more » « less