Dataset Information

Dispersal timing and drought history influence the response of bacterioplankton to drying-rewetting stress.

ABSTRACT: The extent and frequency of drought episodes is expected to increase in the following decades making it a crucial stress factor for smaller water bodies. However, very little is known about how bacterioplankton is affected by increased evaporation and how these communities reassemble after rewetting. Here, we present results from a microcosm experiment that assessed the effect of drying-rewetting stress on bacterioplankton in the light of the stress history and the rate and timing of dispersal after the rewetting. We found that the drying phase resulted mainly in a change of function, whereas the complete desiccation and rewetting processes strongly affected both composition and function, which were, however, influenced by the initial conditions and stress history of the communities. Effects of dispersal were generally stronger when it occurred at an early stage after the rewetting. At this stage, selective establishment of dispersed bacteria coupled with enhanced compositional and functional recovery was found, whereas effects of dispersal were neutral, that is, predictable by dispersal rates, at later stages. Our studies therefore show that both the stress history and the timing of dispersal are important factors that influence the response of bacterial communities to environmental change and stress events.

SUBMITTER: Szekely AJ

PROVIDER: S-EPMC5520042 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

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Dispersal timing and drought history influence the response of bacterioplankton to drying-rewetting stress.

Székely Anna J AJ Langenheder Silke S

The ISME journal 20170425 8

The extent and frequency of drought episodes is expected to increase in the following decades making it a crucial stress factor for smaller water bodies. However, very little is known about how bacterioplankton is affected by increased evaporation and how these communities reassemble after rewetting. Here, we present results from a microcosm experiment that assessed the effect of drying-rewetting stress on bacterioplankton in the light of the stress history and the rate and timing of dispersal a ...[more]

PMID: 28440801

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Project description:Microbiomes contribute to multiple ecosystem services by transforming organic matter in the soil. Extreme shifts in the environment, such as drying-rewetting cycles during drought, can impact the microbial metabolism of organic matter by altering microbial physiology and function. These physiological responses are mediated in part by lipids that are responsible for regulating interactions between cells and the environment. Despite this critical role in regulating the microbial response to stress, little is known about microbial lipids and metabolites in the soil or how they influence phenotypes that are expressed under drying-rewetting cycles. To address this knowledge gap, we conducted a soil incubation experiment to simulate soil drying during a summer drought of an arid grassland, then measured the response of the soil lipidome and metabolome during the first 3 h after wet-up. Reduced nutrient access during soil drying incurred a replacement of membrane phospholipids, resulting in a diminished abundance of multiple phosphorus-rich membrane lipids. The hot and dry conditions increased the prevalence of sphingolipids and lipids containing long-chain polyunsaturated fatty acids, both of which are associated with heat and osmotic stress-mitigating properties in fungi. This novel finding suggests that lipids commonly present in eukaryotes such as fungi may play a significant role in supporting community resilience displayed by arid land soil microbiomes during drought. As early as 10 min after rewetting dry soil, distinct changes were observed in several lipids that had bacterial signatures including a rapid increase in the abundance of glycerophospholipids with saturated and short fatty acid chains, prototypical of bacterial membrane lipids. Polar metabolites including disaccharides, nucleic acids, organic acids, inositols, and amino acids also increased in abundance upon rewetting. This rapid metabolic reactivation and growth after rewetting coincided with an increase in the relative abundance of firmicutes, suggesting that members of this phylum were positively impacted by rewetting. Our study revealed specific changes in lipids and metabolites that are indicative of stress adaptation, substrate use, and cellular recovery during soil drying and subsequent rewetting. The drought-induced nutrient limitation was reflected in the lipidome and polar metabolome, both of which rapidly shifted (within hours) upon rewet. Reduced nutrient access in dry soil caused the replacement of glycerophospholipids with phosphorus-free lipids and impeded resource-expensive osmolyte accumulation. Elevated levels of ceramides and lipids with long-chain polyunsaturated fatty acids in dry soil suggest that lipids likely play an important role in the drought tolerance of microbial taxa capable of synthesizing these lipids. An increasing abundance of bacterial glycerophospholipids and triacylglycerols with fatty acids typical of bacteria and polar metabolites suggest a metabolic recovery in representative bacteria once the environmental conditions are conducive for growth. These results underscore the importance of the soil lipidome as a robust indicator of microbial community responses, especially at the short time scales of cell-environment reactions. Video Abstract.

Project description:Forest soil ecosystems are associated with large pools and fluxes of carbon (C) and nitrogen (N), which could be strongly affected by variation in rainfall events under current climate change. Understanding how dry and wet cycle events might influence the metabolic state of indigenous soil microbes is crucial for predicting forest soil responses to environmental change. We used 454 pyrosequencing and quantitative PCR to address how present (DNA-based) and potentially active (RNA-based) soil bacterial communities might response to the changes in water availability across three different forest types located in two continents (Africa and Asia) under controlled drying and rewetting cycles. Sequencing of rRNA gene and transcript indicated that Proteobacteria, Actinobacteria, and Acidobacteria were the most responsive phyla to changes in water availability. We defined the ratio of rRNA transcript to rRNA gene abundance as a key indicator of potential microbial activity and we found that this ratio was increased following soil dry-down process whereas it decreased after soil rewetting. Following rewetting Crenarchaeota-like 16S rRNA gene transcript increased in some forest soils and this was linked to increases in soil nitrate levels suggesting greater nitrification rates under higher soil water availability. Changes in the relative abundance of (1) different microbial phyla and classes, and (2) 16S and amoA genes were found to be site- and taxa-specific and might have been driven by different life-strategies. Overall, we found that, after rewetting, the structure of the present and potentially active bacterial community structure as well as the abundance of bacterial (16S), archaeal (16S) and ammonia oxidizers (amoA), all returned to pre-dry-down levels. This suggests that microbial taxa have the ability to recover from desiccation, a critical response, which will contribute to maintaining microbial biodiversity in harsh ecosystems under environmental perturbations, such as significant changes in water availability.

Dataset Information

Dispersal timing and drought history influence the response of bacterioplankton to drying-rewetting stress.

Publications

Dispersal timing and drought history influence the response of bacterioplankton to drying-rewetting stress.

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