Monitoring Diel Variations of Physiological Status and Bacterial Diversity in an Estuarine Microbial Mat: An Integrated Biomarker Analysis

Villanueva, Laura; Navarrete, Antoni; Urmeneta, Jordi; Geyer, Roland; White, David C.; Guerrero, Ricardo

doi:10.1007/s00248-007-9224-3

Cited by 23 publications

(22 citation statements)

References 46 publications

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“…Apparently, these bacteria supplement their main carbon and electron source, toluene, during the day with organic plant root exudates, which in turn drives PHA synthesis. A similar diurnal pattern has been found in microbial mats, where heterotrophic microorganisms store excess carbon sources produced and excreted from photosynthetic organisms, such as PHAs, and consume them during night (47). The same mechanism seemed to occur in our wetland model.…”

Section: Fig 3 Dynamics Of Different Protein Abundances During the DIsupporting

confidence: 82%

Aerobic Toluene Degraders in the Rhizosphere of a Constructed Wetland Model Show Diurnal Polyhydroxyalkanoate Metabolism

Lünsmann

Kappelmeyer

Taubert

et al. 2016

Appl Environ Microbiol

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Constructed wetlands (CWs) are successfully applied for the treatment of waters contaminated with aromatic compounds. In these systems, plants provide oxygen and root exudates to the rhizosphere and thereby stimulate microbial degradation processes. Root exudation of oxygen and organic compounds depends on photosynthetic activity and thus may show day-night fluctuations. While diurnal changes in CW effluent composition have been observed, information on respective fluctuations of bacterial activity are scarce. We investigated microbial processes in a CW model system treating toluene-contaminated water which showed diurnal oscillations of oxygen concentrations using metaproteomics. Quantitative real-time PCR was applied to assess diurnal expression patterns of genes involved in aerobic and anaerobic toluene degradation. We observed stable aerobic toluene turnover by Burkholderiales during the day and night. Polyhydroxyalkanoate synthesis was upregulated in these bacteria during the day, suggesting that they additionally feed on organic root exudates while reutilizing the stored carbon compounds during the night via the glyoxylate cycle. Although mRNA copies encoding the anaerobic enzyme benzylsuccinate synthase (bssA) were relatively abundant and increased slightly at night, the corresponding protein could not be detected in the CW model system. Our study provides insights into diurnal patterns of microbial processes occurring in the rhizosphere of an aquatic ecosystem. IMPORTANCEConstructed wetlands are a well-established and cost-efficient option for the bioremediation of contaminated waters. While it is commonly accepted knowledge that the function of CWs is determined by the interplay of plants and microorganisms, the detailed molecular processes are considered a black box. Here, we used a well-characterized CW model system treating toluenecontaminated water to investigate the microbial processes influenced by diurnal plant root exudation. Our results indicated stable aerobic toluene degradation by members of the Burkholderiales during the day and night. Polyhydroxyalkanoate synthesis in these bacteria was higher during the day, suggesting that they additionally fed on organic root exudates and reutilized the stored carbon compounds during the night. Our study illuminates microbial processes occurring in the rhizosphere of an aquatic ecosystem. C onstructed wetlands (CWs) are well-established treatment systems for the bioremediation of contaminated waters (1), including industrial effluents originating from petroleum refineries and their associated contaminated sites (2, 3). Aromatic hydrocarbons present in those wastewaters can effectively be removed in CWs (4-7), largely driven by the interplay of plant physiology and microbial degradation processes in the rhizosphere (8, 9). As in any planted habitat, the rhizosphere of CWs is a complex environment with increased abundance and activity of microorganisms compared to those in the surrounding zones (10). It is shaped by the roots and plant-derived exu...

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Section: Fig 3 Dynamics Of Different Protein Abundances During the DIsupporting

confidence: 82%

Aerobic Toluene Degraders in the Rhizosphere of a Constructed Wetland Model Show Diurnal Polyhydroxyalkanoate Metabolism

Lünsmann

Kappelmeyer

Taubert

et al. 2016

Appl Environ Microbiol

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“…A diel pattern of PHA production in the microbial mats of anaerobic bacteria was reported previously (42). With external carbon sources such as acetate, lactate, and propionate, PHA production by anaerobic purple sulfur bacteria growing with light could be two to five times higher than that in the dark (32).…”

Section: Discussionsupporting

confidence: 66%

Formation of Polyhydroxyalkanoate in Aerobic Anoxygenic Phototrophic Bacteria and Its Relationship to Carbon Source and Light Availability

Xiao

Jiao

2011

Appl Environ Microbiol

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Aerobic anoxygenic phototrophic bacteria (AAPB) are unique players in carbon cycling in the ocean. Cellular carbon storage is an important mechanism regulating the nutrition status of AAPB but is not yet well understood. In this paper, six AAPB species (Dinoroseobacter sp. JL1447, Roseobacter denitrificans OCh 114, Roseobacter litoralis OCh 149, Dinoroseobacter shibae DFL 12 T , Labrenzia alexandrii DFL 11 T , and Erythrobacter longus DSMZ 6997) were examined, and all of them demonstrated the ability to form the carbon polymer polyhydroxyalkanoate (PHA) in the cell. The PHA in Dinoroseobacter sp. JL1447 was identified as poly-betahydroxybutyrate (PHB) according to evidence from Fourier transform infrared spectroscopy, differential scanning calorimetry, and 1 H nuclear magnetic resonance spectroscopy examinations. Carbon sources turned out to be critical for PHA production in AAPB. Among the eight media tested with Dinoroseobacter sp. JL1447, sodium acetate, giving a PHA production rate of 72%, was the most productive carbon source, followed by glucose, with a 68% PHA production rate. Such PHA production rates are among the highest recorded for all bacteria. The C/N ratio of substrates was verified by the experiments as another key factor in PHA production. In the case of R. denitrificans OCh 114, PHA was not detected when the organism was cultured at C/N ratios of <2 but became apparent at C/N ratios of >3. Light is also important for the formation of PHA in AAPB. In the case of Dinoroseobacter sp. JL1447, up to a one-quarter increase in PHB production was observed when the culture underwent growth in a light-dark cycle compared to growth completely in the dark.

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“…form biofilms in beach sand (Piggot et al, 2012), whilst non-pathogenic E. coli are known to persist or even grow within coastal and estuarine environments, particularly in tropical/subtropical climates (Byappanahalli and Fujioka, 1998) and non-pathogenic Clostridium spp. have been isolated from an estuarine mudflat (Villanueva et al, 2007). At locations where significant fecal contamination occurs, FIOs/pathogens can colonize existing biofilm communities.…”

Section: Sediment Characteristics Governing Bacteria Particle Interacmentioning

confidence: 99%

Abundance and Distribution of Enteric Bacteria and Viruses in Coastal and Estuarine Sediments—a Review

et al. 2016

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The long term survival of fecal indicator organisms (FIOs) and human pathogenic microorganisms in sediments is important from a water quality, human health and ecological perspective. Typically, both bacteria and viruses strongly associate with particulate matter present in freshwater, estuarine and marine environments. This association tends to be stronger in finer textured sediments and is strongly influenced by the type and quantity of clay minerals and organic matter present. Binding to particle surfaces promotes the persistence of bacteria in the environment by offering physical and chemical protection from biotic and abiotic stresses. How bacterial and viral viability and pathogenicity is influenced by surface attachment requires further study. Typically, long-term association with surfaces including sediments induces bacteria to enter a viable-but-non-culturable (VBNC) state. Inherent methodological challenges of quantifying VBNC bacteria may lead to the frequent under-reporting of their abundance in sediments. The implications of this in a quantitative risk assessment context remain unclear. Similarly, sediments can harbor significant amounts of enteric viruses, however, the factors regulating their persistence remains poorly understood. Quantification of viruses in sediment remains problematic due to our poor ability to recover intact viral particles from sediment surfaces (typically <10%), our inability to distinguish between infective and damaged (non-infective) viral particles, aggregation of viral particles, and inhibition during qPCR. This suggests that the true viral titre in sediments may be being vastly underestimated. In turn, this is limiting our ability to understand the fate and transport of viruses in sediments. Model systems (e.g., human cell culture) are also lacking for some key viruses, preventing our ability to evaluate the infectivity of viruses recovered from sediments (e.g., norovirus). The release of particle-bound bacteria and viruses into the water column during sediment resuspension also represents a risk to water quality. In conclusion, our poor process level understanding of viral/bacterial-sediment interactions combined with methodological challenges is limiting the accurate source apportionment and quantitative microbial risk assessment for pathogenic organisms associated with sediments in aquatic environments.

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Monitoring Diel Variations of Physiological Status and Bacterial Diversity in an Estuarine Microbial Mat: An Integrated Biomarker Analysis

Cited by 23 publications

References 46 publications

Aerobic Toluene Degraders in the Rhizosphere of a Constructed Wetland Model Show Diurnal Polyhydroxyalkanoate Metabolism

Aerobic Toluene Degraders in the Rhizosphere of a Constructed Wetland Model Show Diurnal Polyhydroxyalkanoate Metabolism

Formation of Polyhydroxyalkanoate in Aerobic Anoxygenic Phototrophic Bacteria and Its Relationship to Carbon Source and Light Availability

Abundance and Distribution of Enteric Bacteria and Viruses in Coastal and Estuarine Sediments—a Review

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