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Elevated temperature alters proteomic responses of individual organisms within a biofilm community.

ABSTRACT: Microbial communities that underpin global biogeochemical cycles will likely be influenced by elevated temperature associated with environmental change. Here, we test an approach to measure how elevated temperature impacts the physiology of individual microbial groups in a community context, using a model microbial-based ecosystem. The study is the first application of tandem mass tag (TMT)-based proteomics to a microbial community. We accurately, precisely and reproducibly quantified thousands of proteins in biofilms growing at 40, 43 and 46?°C. Elevated temperature led to upregulation of proteins involved in amino-acid metabolism at the level of individual organisms and the entire community. Proteins from related organisms differed in their relative abundance and functional responses to temperature. Elevated temperature repressed carbon fixation proteins from two Leptospirillum genotypes, whereas carbon fixation proteins were significantly upregulated at higher temperature by a third member of this genus. Leptospirillum group III bacteria may have been subject to viral stress at elevated temperature, which could lead to greater carbon turnover in the microbial food web through the release of viral lysate. Overall, these findings highlight the utility of proteomics-enabled community-based physiology studies, and provide a methodological framework for possible extension to additional mixed culture and environmental sample analyses.

SUBMITTER: Mosier AC

PROVIDER: S-EPMC4274423 | biostudies-literature | 2015 Jan

REPOSITORIES: biostudies-literature

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Elevated temperature alters proteomic responses of individual organisms within a biofilm community.

Mosier Annika C AC Li Zhou Z Thomas Brian C BC Hettich Robert L RL Pan Chongle C Banfield Jillian F JF

The ISME journal 20140722 1

Microbial communities that underpin global biogeochemical cycles will likely be influenced by elevated temperature associated with environmental change. Here, we test an approach to measure how elevated temperature impacts the physiology of individual microbial groups in a community context, using a model microbial-based ecosystem. The study is the first application of tandem mass tag (TMT)-based proteomics to a microbial community. We accurately, precisely and reproducibly quantified thousands ...[more]

PMID: 25050524

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Project description:BACKGROUND: Atlantic salmon aquaculture operations in the Northern hemisphere experience large seasonal fluctuations in seawater temperature. With summer temperatures often peaking around 18-20°C there is growing concern about the effects on fish health and performance. Since the heart has a major role in the physiological plasticity and acclimation to different thermal conditions in fish, we wanted to investigate how three and eight weeks exposure of adult Atlantic salmon to 19°C, previously shown to significantly reduce growth performance, affected expression of relevant genes and proteins in cardiac tissues under experimental conditions. RESULTS: Transcriptional responses in cardiac tissues after three and eight weeks exposure to 19°C (compared to thermal preference, 14°C) were analyzed with cDNA microarrays and validated by expression analysis of selected genes and proteins using real-time qPCR and immunofluorescence microscopy. Up-regulation of heat shock proteins and cell signaling genes may indicate involvement of the unfolded protein response in long-term acclimation to elevated temperature. Increased immunofluorescence staining of inducible nitric oxide synthase in spongy and compact myocardium as well as increased staining of vascular endothelial growth factor in epicardium could reflect induced vascularization and vasodilation, possibly related to increased oxygen demand. Increased staining of collagen I in the compact myocardium of 19°C fish may be indicative of a remodeling of connective tissue with long-term warm acclimation. Finally, higher abundance of transcripts for genes involved in innate cellular immunity and lower abundance of transcripts for humoral immune components implied altered immune competence in response to elevated temperature. CONCLUSIONS: Long-term exposure of Atlantic salmon to 19°C resulted in cardiac gene and protein expression changes indicating that the unfolded protein response, vascularization, remodeling of connective tissue and altered innate immune responses were part of the cardiac acclimation or response to elevated temperature.

Project description:Anode-associated multispecies exoelectrogenic biofilms are essential for the function of bioelectrochemical systems (BESs). The individual activities of anode-associated organisms and physiological responses resulting from coculturing are often hard to assess due to the high microbial diversity in these systems. Therefore, we developed a model multispecies biofilm comprising three exoelectrogenic proteobacteria, Shewanella oneidensis, Geobacter sulfurreducens, and Geobacter metallireducens, with the aim to study in detail the biofilm formation dynamics, the interactions between the organisms, and the overall activity of an exoelectrogenic biofilm as a consequence of the applied anode potential. The experiments revealed that the organisms build a stable biofilm on an electrode surface that is rather resilient to changes in the redox potential of the anode. The community operated at maximum electron transfer rates at electrode potentials that were higher than 0.04 V versus a normal hydrogen electrode. Current densities decreased gradually with lower potentials and reached half-maximal values at -0.08 V. Transcriptomic results point toward a positive interaction among the individual strains. S. oneidensis and G. sulfurreducens upregulated their central metabolisms as a response to cultivation under mixed-species conditions. G. sulfurreducens was detected in the planktonic phase of the bioelectrochemical reactors in mixed-culture experiments but not when it was grown in the absence of the other two organisms.IMPORTANCE In many cases, multispecies communities can convert organic substrates into electric power more efficiently than axenic cultures, a phenomenon that remains unresolved. In this study, we aimed to elucidate the potential mutual effects of multispecies communities in bioelectrochemical systems to understand how microbes interact in the coculture anodic network and to improve the community's conversion efficiency for organic substrates into electrical energy. The results reveal positive interactions that might lead to accelerated electron transfer in mixed-species anode communities. The observations made within this model biofilm might be applicable to a variety of nonaxenic systems in the field.

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Elevated temperature alters proteomic responses of individual organisms within a biofilm community.

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Elevated temperature alters proteomic responses of individual organisms within a biofilm community.

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