Publications by authors named "Paul L E Bodelier"

72 Publications

Complete and Draft Genome Sequences of Aerobic Methanotrophs Isolated from a Riparian Wetland.

Microbiol Resour Announc 2021 Mar 4;10(9). Epub 2021 Mar 4.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands

Wetlands are important sources of methane emissions, and the impacts of these emissions can be mitigated by methanotrophic bacteria. The genomes of methanotrophs sp. strain LL1 and sp. strain H3A, as well as sp. strains H4A, H15, H62, and L43, were sequenced and are reported here.
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http://dx.doi.org/10.1128/MRA.01438-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7936639PMC
March 2021

Response of a methane-driven interaction network to stressor intensification.

FEMS Microbiol Ecol 2020 10;96(10)

Institute of Microbiology, Leibniz Universität Hannover, Herrenhäuser Str. 2, 30419 Hannover, Germany.

Microorganisms may reciprocally select for specific interacting partners, forming a network with interdependent relationships. The methanotrophic interaction network, comprising methanotrophs and non-methanotrophs, is thought to modulate methane oxidation and give rise to emergent properties beneficial for the methanotrophs. Therefore, microbial interaction may become relevant for community functioning under stress. However, empirical validation of the role and stressor-induced response of the interaction network remains scarce. Here, we determined the response of a complex methane-driven interaction network to a stepwise increase in NH4Cl-induced stress (0.5-4.75 g L-1, in 0.25-0.5 g L-1 increments) using enrichment of a naturally occurring complex community derived from a paddy soil in laboratory-scale incubations. Although ammonium and intermediates of ammonium oxidation are known to inhibit methane oxidation, methanotrophic activity was unexpectedly detected even in incubations with high ammonium levels, albeit rates were significantly reduced. Sequencing analysis of the 16S rRNA and pmoA genes consistently revealed divergent communities in the reference and stressed incubations. The 16S rRNA-based co-occurrence network analysis revealed that NH4Cl-induced stress intensification resulted in a less complex and modular network, likely driven by less stable interaction. Interestingly, the non-methanotrophs formed the key nodes, and appear to be relevant members of the community. Overall, stressor intensification unravels the interaction network, with adverse consequences for community functioning.
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http://dx.doi.org/10.1093/femsec/fiaa180DOI Listing
October 2020

Grand Challenges in Terrestrial Microbiology: Moving on From a Decade of Progress in Microbial Biogeochemistry.

Front Microbiol 2020 15;11:981. Epub 2020 May 15.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, Netherlands.

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http://dx.doi.org/10.3389/fmicb.2020.00981DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7243610PMC
May 2020

Niche Differentiation of Host-Associated Pelagic Microbes and Their Potential Contribution to Biogeochemical Cycling in Artificially Warmed Lakes.

Front Microbiol 2020 23;11:582. Epub 2020 Apr 23.

Department of Microbial Ecology, Netherlands Institute of Ecology, Wageningen, Netherlands.

It has been proposed that zooplankton-associated microbes provide numerous beneficial services to their "host". However, there is still a lack of understanding concerning the effect of temperature on the zooplankton microbiome. Furthermore, it is unclear to what extent the zooplankton microbiome differs from free-living and particle-associated (PA) microbes. Here, we explicitly addressed these issues by investigating (1) the differences in free-living, PA, and zooplankton associated microbes and (2) the impact of temperature on these microbes in the water column of a series of lakes artificially warmed by two power plants. High-throughput amplicon sequencing of the 16S rRNA gene showed that diversity and composition of the bacterial community associated to zooplankton, PA, and bacterioplankton varied significantly from one another, grouping in different clusters indicating niche differentiation of pelagic microbes. From the abiotic parameters measured, temperature significantly affected the diversity and composition of all analyzed microbiomes. Two phyla (e.g., Proteobacteria and Bacteroidetes) dominated in zooplankton microbiomes whereas Actinobacteria was the dominant phylum in the bacterioplankton. The microbial species richness and diversity was lower in zooplankton compared to bacterioplankton and PA. Surprisingly, genera of methane-oxidizing bacteria, methylotrophs and nitrifiers (e.g., ) significantly associated with the microbiome of zooplankton and PA. Our study clearly demonstrates niche differentiation of pelagic microbes and their potential link to biogeochemical cycling in freshwater systems.
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http://dx.doi.org/10.3389/fmicb.2020.00582DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7190982PMC
April 2020

Can flooding-induced greenhouse gas emissions be mitigated by trait-based plant species choice?

Sci Total Environ 2020 Jul 10;727:138476. Epub 2020 Apr 10.

Soil Biology Group, Wageningen University & Research, PO Box 47, 6700 AA Wageningen, the Netherlands; Department of Agroecology - Soil Fertility, Aarhus University, Blichers Allé 20, 8830 Tjele, Denmark.

Intensively managed grasslands are large sources of the potent greenhouse gas nitrous oxide (NO) and important regulators of methane (CH) consumption and production. The predicted increase in flooding frequency and severity due to climate change could increase NO emissions and shift grasslands from a net CH sink to a source. Therefore, effective management strategies are critical for mitigating greenhouse gas emissions from flood-prone grasslands. We tested how repeated flooding affected the NO and CH emissions from 11 different plant communities (Festuca arundinacea, Lolium perenne, Poa trivialis, and Trifolium repens in monoculture, 2- and 4-species mixtures), using intact soil cores from an 18-month old grassland field experiment in a 4-month greenhouse experiment. To elucidate potential underlying mechanisms, we related plant functional traits to cumulative NO and CH emissions. We hypothesized that traits related with fast nitrogen uptake and growth would lower NO and CH emissions in ambient (non-flooded) conditions, and that traits related to tissue toughness would lower NO and CH emissions in flooded conditions. We found that flooding increased cumulative NO emissions by 97 fold and cumulative CH emissions by 1.6 fold on average. Plant community composition mediated the flood-induced increase in NO emissions. In flooded conditions, increasing abundance of the grass F. arundinacea was related with lower NO emissions; whereas increases in abundance of the legume T. repens resulted in higher NO emissions. In non-flooded conditions, NO emissions were not clearly mediated by plant traits related with nitrogen uptake or biomass production. In flooded conditions, plant communities with high root carbon to nitrogen ratio were related with lower cumulative NO emissions, and a lower global warming potential (CO equivalent of NO and CH). We conclude that plant functional traits related to slower decomposition and nitrogen mineralization could play a significant role in mitigating NO emissions in flooded grasslands.
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http://dx.doi.org/10.1016/j.scitotenv.2020.138476DOI Listing
July 2020

Co-occurrence patterns among prokaryotes across an age gradient in pit mud of Chinese strong-flavor liquor.

Can J Microbiol 2020 Sep 1;66(9):495-504. Epub 2020 Apr 1.

School of Food and Biological Engineering, Zhengzhou University of Light Industry, Zhengzhou 450002, Henan Province, People's Republic of China.

It is widely believed that the quality and characteristics of Chinese strong-flavor liquor (CSFL) are closely related to the age of the pit mud; CSFL produced from older pit mud tastes better. This study aimed to investigate the alteration and interaction of prokaryotic communities across an age gradient in pit mud. Prokaryotic microbes in different-aged pit mud (1, 6, and 10 years old) were analyzed by Illumina MiSeq sequencing of the 16S rRNA gene. Analysis of the 16S rRNA gene indicated that the prokaryotic community was significantly altered with pit mud age. There was a significant increase in the genera , , and with increased age of pit mud, while the genus showed a significant decreasing trend. Network analysis demonstrated that both synergetic co-occurrence and niche competition were dominated by 68 prokaryotic genera. These genera formed 10 hubs of co-occurrence patterns, mainly under the phyla , , and , playing important roles on ecosystem stability of the pit mud. Environmental variables (pH, NH, available P, available K, and Ca) correlated significantly with prokaryotic community assembly. The interaction of prokaryotic communities in the pit mud ecosystem and the relationship among prokaryotic communities and environmental factors contribute to the higher quality of the pit mud in older fermentation pits.
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http://dx.doi.org/10.1139/cjm-2020-0012DOI Listing
September 2020

Strain C50C1 Is a Novel Type Ib Gammaproteobacterial Methanotroph Adapted to Freshwater Environments.

mSphere 2019 06 5;4(3). Epub 2019 Jun 5.

Department of Microbiology, IWWR, Radboud University, Nijmegen, the Netherlands.

Methane-oxidizing microorganisms perform an important role in reducing emissions of the greenhouse gas methane to the atmosphere. To date, known bacterial methanotrophs belong to the , , and NC10 phyla. Within the phylum, they can be divided into type Ia, type Ib, and type II methanotrophs. Type Ia and type II are well represented by isolates. Contrastingly, the vast majority of type Ib methanotrophs have not been able to be cultivated so far. Here, we compared the distributions of type Ib lineages in different environments. Whereas the cultivated type Ib methanotrophs ( and ) are found in landfill and upland soils, lineages that are not represented by isolates are mostly dominant in freshwater environments, such as paddy fields and lake sediments. Thus, we observed a clear niche differentiation within type Ib methanotrophs. Our subsequent isolation attempts resulted in obtaining a pure culture of a novel type Ib methanotroph, tentatively named "" C50C1. Strain C50C1 was further characterized to be an obligate methanotroph, containing Cω9c as the major membrane phospholipid fatty acid, which has not been found in other methanotrophs. Genome analysis of strain C50C1 showed the presence of two operon copies and XoxF5-type methanol dehydrogenase in addition to MxaFI. The genome also contained genes involved in nitrogen and sulfur cycling, but it remains to be demonstrated if and how these help this type Ib methanotroph to adapt to fluctuating environmental conditions in freshwater ecosystems. Most of the methane produced on our planet gets naturally oxidized by a group of methanotrophic microorganisms before it reaches the atmosphere. These microorganisms are able to oxidize methane, both aerobically and anaerobically, and use it as their sole energy source. Although methanotrophs have been studied for more than a century, there are still many unknown and uncultivated groups prevalent in various ecosystems. This study focused on the diversity and adaptation of aerobic methane-oxidizing bacteria in different environments by comparing their phenotypic and genotypic properties. We used lab-scale microcosms to create a countergradient of oxygen and methane for preenrichment, followed by classical isolation techniques to obtain methane-oxidizing bacteria from a freshwater environment. This resulted in the discovery and isolation of a novel methanotroph with interesting physiological and genomic properties that could possibly make this bacterium able to cope with fluctuating environmental conditions.
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http://dx.doi.org/10.1128/mSphere.00631-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6553558PMC
June 2019

Organic Residue Amendments to Modulate Greenhouse Gas Emissions From Agricultural Soils.

Front Microbiol 2018 7;9:3035. Epub 2018 Dec 7.

Department of Microbial Ecology Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, Netherlands.

Organic fertilizers have been shown to stimulate CH uptake from agricultural soils. Managing fertilizer application to maximize this effect and to minimize emission of other greenhouse gasses offers possibilities to increase sustainability of agriculture. To tackle this challenge, we incubated an agricultural soil with different organic amendments (compost, sewage sludge, digestate, cover crop residues mixture), either as single application or in a mixture and subjected it to different soil moisture concentrations using different amounts of organic amendments. GHG fluxes and CH oxidation rates were measured repeatedly, while changes in organic matter and abundance of GHG relevant microbial groups (nitrifiers, denitrifiers, methanotrophs, methanogens) were measured at the end of the incubation. Overall the dynamics of the analyzed GHGs differed significantly. While CO and NO differed considerably between the treatments, CH fluxes remained stable. In contrast, CH oxidation showed a clear increase for all amendments over time. CO fluxes were mostly dependent on the amount of organic residue that was used, while NO fluxes were affected more by soil moisture. Several combinations of amendments led to reductions of CO, CH, and/or NO emissions compared to un-amended soil. Most optimal GHG balance was obtained by compost amendments, which resulted in a similar overall GHG balance as compared to the un-amended soil. However, compost is not very nutrient rich potentially leading to lower crop yield when applied as single fertilizer. Hence, the combination of compost with one of the more nutrient rich organic amendments (sewage sludge, digestate) provides a trade-off between maintaining crop yield and minimizing GHG emissions. Additionally, we could observe a strong increase in microbial communities involved in GHG consumption in all amendments, with the strongest increase associated with cover crop residue mixtures. Future research should focus on the interrelation of plants, soil, and microbes and their impact on the global warming potential in relation to applied organic amendments.
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http://dx.doi.org/10.3389/fmicb.2018.03035DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6292959PMC
December 2018

Modulation of Litter Decomposition by the Soil Microbial Food Web Under Influence of Land Use Change.

Front Microbiol 2018 26;9:2860. Epub 2018 Nov 26.

Institute of Environmental Biology, Utrecht University, Utrecht, Netherlands.

Soil microbial communities modulate soil organic matter (SOM) dynamics by catalyzing litter decomposition. However, our understanding of how litter-derived carbon (C) flows through the microbial portion of the soil food web is far from comprehensive. This information is necessary to facilitate reliable predictions of soil C cycling and sequestration in response to a changing environment such as land use change in the form of agricultural abandonment. To examine the flow of litter-derived C through the soil microbial food web and it's response to land use change, we carried out an incubation experiment with soils from six fields; three recently abandoned and three long term abandoned fields. In these soils, the fate of C-labeled plant litter was followed by analyzing phospholipid fatty acids (PLFA) over a period of 56 days. The litter-amended soils were sampled over time to measure CO and mineral N dynamics. Microbial C-incorporation patterns revealed a clear succession of microbial groups during litter decomposition. Fungi were first to incorporate C-label, followed by G bacteria, G bacteria, actinomycetes and micro-fauna. The order in which various microbial groups responded to litter decomposition was similar across all the fields examined, with no clear distinction between recent and long-term abandoned soils. Although the microbial biomass was initially higher in long-term abandoned soils, the net amount of C-labeled litter that was incorporated by the soil microbial community was ultimately comparable between recent and long-term abandoned fields. In relative terms, this means there was a higher efficiency of litter-derived C-incorporation in recent abandoned soil microbial communities compared to long-term abandoned soils, most likely due to a net shift from SOM-derived C toward root-derived C input in the soil microbial food web following land-abandonment.
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http://dx.doi.org/10.3389/fmicb.2018.02860DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6275175PMC
November 2018

Ethyl tert-butyl ether (EtBE) degradation by an algal-bacterial culture obtained from contaminated groundwater.

Water Res 2019 01 22;148:314-323. Epub 2018 Oct 22.

Deltares, Subsurface and Groundwater Systems, Daltonlaan 600, 3584 BK, Utrecht, the Netherlands.

EtBE is a fuel oxygenate that is synthesized from (bio)ethanol and fossil-based isobutylene, and replaces the fossil-based MtBE. Biodegradation of EtBE to harmless metabolites or end products can reduce the environmental and human health risks after accidental release. In this study, an algal-bacterial culture enriched from contaminated groundwater was used to (i) assess the potential for EtBE degradation, (ii) resolve the EtBE degradation pathway and (iii) characterize the phylogenetic composition of the bacterial community involved in EtBE degradation in contaminated groundwater. In an unamended microcosm, algal growth was observed after eight weeks when exposed to a day-night light cycle. In the fed-batch reactor, oxygen produced by the algae Scenedesmus and Chlorella was used by bacteria to degrade 50 μM EtBE replenishments with a cumulative total of 1250 μM in a day/night cycle (650 lux), over a period of 913 days. The microbial community in the fed-batch reactor degraded EtBE, using a P450 monooxygenase and 2-hydroxyisobutyryl-CoA mutase, to tert-butyl alcohol (TBA), ethanol and CO as determined using C nuclear magnetic resonance spectroscopy (NMR) and gas chromatography. Stable isotope probing (SIP) with C labeled EtBE in a fed-batch vessel showed no significant difference in community profiles of the C and C enriched DNA fractions, with representatives of the families Halomonadaceae, Shewanellaceae, Rhodocyclaceae, Oxalobacteraceae, Comamonadaceae, Sphingomonadaceae, Hyphomicrobiaceae, Candidatus Moranbacteria, Omnitrophica, Anaerolineaceae, Nocardiaceae, and Blastocatellaceae. This is the first study describing micro-oxic degradation of EtBE by an algal-bacterial culture. This algal-bacterial culture has advantages compared with conventional aerobic treatments: (i) a lower risk of EtBE evaporation and (ii) no need for external oxygen supply in the presence of light. This study provides novel leads towards future possibilities to implement algal-bacterial consortia in field-scale groundwater or wastewater treatment.
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http://dx.doi.org/10.1016/j.watres.2018.10.050DOI Listing
January 2019

Resistance and Recovery of Methane-Oxidizing Communities Depends on Stress Regime and History; A Microcosm Study.

Front Microbiol 2018 31;9:1714. Epub 2018 Jul 31.

Department Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, Netherlands.

Although soil microbes are responsible for important ecosystem functions, and soils are under increasing environmental pressure, little is known about their resistance and resilience to multiple stressors. Here, we test resistance and recovery of soil methane-oxidizing communities to two different, repeated, perturbations: soil drying, ammonium addition and their combination. In replicated soil microcosms we measured methane oxidation before and after perturbations, while monitoring microbial abundance and community composition using quantitative PCR assays for the bacterial 16S rRNA and gene, and sequencing of the bacterial 16S rRNA gene. Although microbial community composition changed after soil drying, methane oxidation rates recovered, even after four desiccation events. Moreover, microcosms subjected to soil drying recovered significantly better from ammonium addition compared to microcosms not subjected to soil drying. Our results show the flexibility of microbial communities, even if abundances of dominant populations drop, ecosystem functions can recover. In addition, a history of stress may induce changes in community composition and functioning, which may in turn affect its future tolerance to different stressors.
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http://dx.doi.org/10.3389/fmicb.2018.01714DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6080070PMC
July 2018

Environmental legacy contributes to the resilience of methane consumption in a laboratory microcosm system.

Sci Rep 2018 06 11;8(1):8862. Epub 2018 Jun 11.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.

The increase of extreme drought and precipitation events due to climate change will alter microbial processes. Perturbation experiments demonstrated that microbes are sensitive to environmental alterations. However, only little is known on the legacy effects in microbial systems. Here, we designed a laboratory microcosm experiment using aerobic methane-consuming communities as a model system to test basic principles of microbial resilience and the role of changes in biomass and the presence of non-methanotrophic microbes in this process. We focused on enrichments from soil, sediment, and water reflecting communities with different legacy with respect to exposure to drought. Recovery rates, a recently proposed early warning indicator of a critical transition, were utilized as a measure to detect resilience loss of methane consumption during a series of dry/wet cycle perturbations. We observed a slowed recovery of enrichments originating from water samples, which suggests that the community's legacy with a perturbation is a contributing factor for the resilience of microbial functioning.
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http://dx.doi.org/10.1038/s41598-018-27168-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5995846PMC
June 2018

Positive diversity-functioning relationships in model communities of methanotrophic bacteria.

Ecology 2018 03 12;99(3):714-723. Epub 2018 Feb 12.

Department of Evolutionary Biology and Environmental Studies, University of Zürich, Winterthurerstrasse 190, CH-8057, Zurich, Switzerland.

Biodiversity enhances ecosystem functions such as biomass production and nutrient cycling. Although the majority of the terrestrial biodiversity is hidden in soils, very little is known about the importance of the diversity of microbial communities for soil functioning. Here, we tested effects of biodiversity on the functioning of methanotrophs, a specialized group of soil bacteria that plays a key role in mediating greenhouse gas emissions from soils. Using pure strains of methanotrophic bacteria, we assembled artificial communities of different diversity levels, with which we inoculated sterile soil microcosms. To assess the functioning of these communities, we measured methane oxidation by gas chromatography throughout the experiment and determined changes in community composition and community size at several time points by quantitative PCR and sequencing. We demonstrate that microbial diversity had a positive overyielding effect on methane oxidation, in particular at the beginning of the experiment. This higher assimilation of CH at high diversity translated into increased growth and significantly larger communities towards the end of the study. The overyielding of mixtures with respect to CH consumption and community size were positively correlated. The temporal CH consumption profiles of strain monocultures differed, raising the possibility that temporal complementarity of component strains drove the observed community-level strain richness effects; however, the community niche metric we derived from the temporal activity profiles did not explain the observed strain richness effect. The strain richness effect also was unrelated to both the phylogenetic and functional trait diversity of mixed communities. Overall, our results suggest that positive biodiversity-ecosystem-function relationships show similar patterns across different scales and may be widespread in nature. Additionally, biodiversity is probably also important in natural methanotrophic communities for the ecosystem function methane oxidation. Therefore, maintaining soil conditions that support a high diversity of methanotrophs may help to reduce the emission of the greenhouse gas methane.
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http://dx.doi.org/10.1002/ecy.2138DOI Listing
March 2018

Impact of Peat Mining and Restoration on Methane Turnover Potential and Methane-Cycling Microorganisms in a Northern Bog.

Appl Environ Microbiol 2018 02 17;84(3). Epub 2018 Jan 17.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, the Netherlands

Ombrotrophic peatlands are a recognized global carbon reservoir. Without restoration and peat regrowth, harvested peatlands are dramatically altered, impairing their carbon sink function, with consequences for methane turnover. Previous studies determined the impact of commercial mining on the physicochemical properties of peat and the effects on methane turnover. However, the response of the underlying microbial communities catalyzing methane production and oxidation have so far received little attention. We hypothesize that with the return of spp. postharvest, methane turnover potential and the corresponding microbial communities will converge in a natural and restored peatland. To address our hypothesis, we determined the potential methane production and oxidation rates in natural (as a reference), actively mined, abandoned, and restored peatlands over two consecutive years. In all sites, the methanogenic and methanotrophic population sizes were enumerated using quantitative PCR (qPCR) assays targeting the and genes, respectively. Shifts in the community composition were determined using Illumina MiSeq sequencing of the gene and a -based terminal restriction fragment length polymorphism (t-RFLP) analysis, complemented by cloning and sequence analysis of the gene. Peat mining adversely affected methane turnover potential, but the rates recovered in the restored site. The recovery in potential activity was reflected in the methanogenic and methanotrophic abundances. However, the microbial community composition was altered, being more pronounced for the methanotrophs. Overall, we observed a lag between the recovery of the methanogenic/methanotrophic activity and the return of the corresponding microbial communities, suggesting that a longer duration (>15 years) is needed to reverse mining-induced effects on the methane-cycling microbial communities. Ombrotrophic peatlands are a crucial carbon sink, but this environment is also a source of methane, an important greenhouse gas. Methane emission in peatlands is regulated by methane production and oxidation catalyzed by methanogens and methanotrophs, respectively. Methane-cycling microbial communities have been documented in natural peatlands. However, less is known of their response to peat mining and of the recovery of the community after restoration. Mining exerts an adverse impact on potential methane production and oxidation rates and on methanogenic and methanotrophic population abundances. Peat mining also induced a shift in the methane-cycling microbial community composition. Nevertheless, with the return of spp. in the restored site after 15 years, methanogenic and methanotrophic activity and population abundance recovered well. The recovery, however, was not fully reflected in the community composition, suggesting that >15 years are needed to reverse mining-induced effects.
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http://dx.doi.org/10.1128/AEM.02218-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5772240PMC
February 2018

Revisiting life strategy concepts in environmental microbial ecology.

FEMS Microbiol Ecol 2017 03;93(3)

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB Wageningen, The Netherlands.

Microorganisms are physiologically diverse, possessing disparate genomic features and mechanisms for adaptation (functional traits), which reflect on their associated life strategies and determine at least to some extent their prevalence and distribution in the environment. Unlike animals and plants, there is an unprecedented diversity and intractable metabolic versatility among bacteria, making classification or grouping these microorganisms based on their functional traits as has been done in animal and plant ecology challenging. Nevertheless, based on representative pure cultures, microbial traits distinguishing different life strategies had been proposed, and had been the focus of previous reviews. In the environment, however, the vast majority of naturally occurring microorganisms have yet to be isolated, restricting the association of life strategies to broad phylogenetic groups and/or physiological characteristics. Here, we reviewed the literature to determine how microbial life strategy concepts (i.e. copio- and oligotrophic strategists, and competitor-stress tolerator-ruderals framework) are applied in complex microbial communities. Because of the scarcity of direct empirical evidence elucidating the associated life strategies in complex communities, we rely heavily on observational studies determining the response of microorganisms to (a)biotic cues (e.g. resource availability) to infer microbial life strategies. Although our focus is on the life strategies of bacteria, parallels were drawn from the fungal community. Our literature search showed inconsistency in the community response of proposed copiotrophic- and oligotrophic-associated microorganisms (phyla level) to changing environmental conditions. This suggests that tracking microorganisms at finer phylogenetic and taxonomic resolution (e.g. family level or lower) may be more effective to capture changes in community response and/or that edaphic factors exert a stronger effect in community response. We discuss the limitations and provide recommendations for future research applying microbial life strategies in environmental studies.
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http://dx.doi.org/10.1093/femsec/fix006DOI Listing
March 2017

Biotic Interactions in Microbial Communities as Modulators of Biogeochemical Processes: Methanotrophy as a Model System.

Front Microbiol 2016 23;7:1285. Epub 2016 Aug 23.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW) Wageningen, Netherlands.

Microbial interaction is an integral component of microbial ecology studies, yet the role, extent, and relevance of microbial interaction in community functioning remains unclear, particularly in the context of global biogeochemical cycles. While many studies have shed light on the physico-chemical cues affecting specific processes, (micro)biotic controls and interactions potentially steering microbial communities leading to altered functioning are less known. Yet, recent accumulating evidence suggests that the concerted actions of a community can be significantly different from the combined effects of individual microorganisms, giving rise to emergent properties. Here, we exemplify the importance of microbial interaction for ecosystem processes by analysis of a reasonably well-understood microbial guild, namely, aerobic methane-oxidizing bacteria (MOB). We reviewed the literature which provided compelling evidence for the relevance of microbial interaction in modulating methane oxidation. Support for microbial associations within methane-fed communities is sought by a re-analysis of literature data derived from stable isotope probing studies of various complex environmental settings. Putative positive interactions between active MOB and other microbes were assessed by a correlation network-based analysis with datasets covering diverse environments where closely interacting members of a consortium can potentially alter the methane oxidation activity. Although, methanotrophy is used as a model system, the fundamentals of our postulations may be applicable to other microbial guilds mediating other biogeochemical processes.
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http://dx.doi.org/10.3389/fmicb.2016.01285DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4993757PMC
September 2016

Conventional methanotrophs are responsible for atmospheric methane oxidation in paddy soils.

Nat Commun 2016 06 1;7:11728. Epub 2016 Jun 1.

State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, Jiangsu Province 210008, China.

Soils serve as the biological sink of the potent greenhouse gas methane with exceptionally low concentrations of ∼1.84 p.p.m.v. in the atmosphere. The as-yet-uncultivated methane-consuming bacteria have long been proposed to be responsible for this 'high-affinity' methane oxidation (HAMO). Here we show an emerging HAMO activity arising from conventional methanotrophs in paddy soil. HAMO activity was quickly induced during the low-affinity oxidation of high-concentration methane. Activity was lost gradually over 2 weeks, but could be repeatedly regained by flush-feeding the soil with elevated methane. The induction of HAMO activity occurred only after the rapid growth of methanotrophic populations, and a metatranscriptome-wide association study suggests that the concurrent high- and low-affinity methane oxidation was catalysed by known methanotrophs rather than by the proposed novel atmospheric methane oxidizers. These results provide evidence of atmospheric methane uptake in periodically drained ecosystems that are typically considered to be a source of atmospheric methane.
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http://dx.doi.org/10.1038/ncomms11728DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4895445PMC
June 2016

Recurrence and Frequency of Disturbance have Cumulative Effect on Methanotrophic Activity, Abundance, and Community Structure.

Front Microbiol 2015 5;6:1493. Epub 2016 Jan 5.

Department of Microbial Ecology, Netherlands Institute of Ecology Wageningen, Netherlands.

Alternate prolonged drought and heavy rainfall is predicted to intensify with global warming. Desiccation-rewetting events alter the soil quality and nutrient concentrations which drive microbial-mediated processes, including methane oxidation, a key biogeochemical process catalyzed by methanotrophic bacteria. Although aerobic methanotrophs showed remarkable resilience to a suite of physical disturbances induced as a single event, their resilience to recurring disturbances is less known. Here, using a rice field soil in a microcosm study, we determined whether recurrence and frequency of desiccation-rewetting impose an accumulating effect on the methanotrophic activity. The response of key aerobic methanotroph subgroups (type Ia, Ib, and II) were monitored using qPCR assays, and was supported by a t-RFLP analysis. The methanotrophic activity was resilient to recurring desiccation-rewetting, but increasing the frequency of the disturbance by twofold significantly decreased methane uptake rate. Both the qPCR and t-RFLP analyses were congruent, showing the dominance of type Ia/Ib methanotrophs prior to disturbance, and after disturbance, the recovering community was predominantly comprised of type Ia (Methylobacter) methanotrophs. Both type Ib and type II (Methylosinus/Methylocystis) methanotrophs were adversely affected by the disturbance, but type II methanotrophs showed recovery over time, indicating relatively higher resilience to the disturbance. This revealed distinct, yet unrecognized traits among the methanotroph community members. Our results show that recurring desiccation-rewetting before a recovery in community abundance had an accumulated effect, compromising methanotrophic activity. While methanotrophs may recover well following sporadic disturbances, their resilience may reach a 'tipping point' where activity no longer recovered if disturbance persists and increase in frequency.
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http://dx.doi.org/10.3389/fmicb.2015.01493DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4700171PMC
January 2016

Compositional and functional stability of aerobic methane consuming communities in drained and rewetted peat meadows.

FEMS Microbiol Ecol 2015 Nov 7;91(11). Epub 2015 Oct 7.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, 6708 PB, the Netherlands.

The restoration of peatlands is an important strategy to counteract subsidence and loss of biodiversity. However, responses of important microbial soil processes are poorly understood. We assessed functioning, diversity and spatial organization of methanotrophic communities in drained and rewetted peat meadows with different water table management and agricultural practice. Results show that the methanotrophic diversity was similar between drained and rewetted sites with a remarkable dominance of the genus Methylocystis. Enzyme kinetics depicted no major differences, indicating flexibility in the methane (CH4) concentrations that can be used by the methanotrophic community. Short-term flooding led to temporary elevated CH4 emission but to neither major changes in abundances of methane-oxidizing bacteria (MOB) nor major changes in CH4 consumption kinetics in drained agriculturally used peat meadows. Radiolabeling and autoradiographic imaging of intact soil cores revealed a markedly different spatial arrangement of the CH4 consuming zone in cores exposed to near-atmospheric and elevated CH4. The observed spatial patterns of CH4 consumption in drained peat meadows with and without short-term flooding highlighted the spatial complexity and responsiveness of the CH4 consuming zone upon environmental change. The methanotrophic microbial community is not generally altered and harbors MOB that can cover a large range of CH4 concentrations offered due to water-table fluctuations, effectively mitigating CH4 emissions.
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http://dx.doi.org/10.1093/femsec/fiv119DOI Listing
November 2015

Sustainability: Bypassing the methane cycle.

Nature 2015 Jul 22;523(7562):534-5. Epub 2015 Jul 22.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), 6708 PB Wageningen, the Netherlands.

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http://dx.doi.org/10.1038/nature14633DOI Listing
July 2015

Unexpected stimulation of soil methane uptake as emergent property of agricultural soils following bio-based residue application.

Glob Chang Biol 2015 Oct 27;21(10):3864-79. Epub 2015 Jun 27.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708, PB Wageningen, The Netherlands.

Intensification of agriculture to meet the global food, feed, and bioenergy demand entail increasing re-investment of carbon compounds (residues) into agro-systems to prevent decline of soil quality and fertility. However, agricultural intensification decreases soil methane uptake, reducing, and even causing the loss of the methane sink function. In contrast to wetland agricultural soils (rice paddies), the methanotrophic potential in well-aerated agricultural soils have received little attention, presumably due to the anticipated low or negligible methane uptake capacity in these soils. Consequently, a detailed study verifying or refuting this assumption is still lacking. Exemplifying a typical agricultural practice, we determined the impact of bio-based residue application on soil methane flux, and determined the methanotrophic potential, including a qualitative (diagnostic microarray) and quantitative (group-specific qPCR assays) analysis of the methanotrophic community after residue amendments over 2 months. Unexpectedly, after amendments with specific residues, we detected a significant transient stimulation of methane uptake confirmed by both the methane flux measurements and methane oxidation assay. This stimulation was apparently a result of induced cell-specific activity, rather than growth of the methanotroph population. Although transient, the heightened methane uptake offsets up to 16% of total gaseous CO2 emitted during the incubation. The methanotrophic community, predominantly comprised of Methylosinus may facilitate methane oxidation in the agricultural soils. While agricultural soils are generally regarded as a net methane source or a relatively weak methane sink, our results show that methane oxidation rate can be stimulated, leading to higher soil methane uptake. Hence, even if agriculture exerts an adverse impact on soil methane uptake, implementing carefully designed management strategies (e.g. repeated application of specific residues) may compensate for the loss of the methane sink function following land-use change.
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http://dx.doi.org/10.1111/gcb.12974DOI Listing
October 2015

Phylogenetic Characterization of Phosphatase-Expressing Bacterial Communities in Baltic Sea Sediments.

Microbes Environ 2015 28;30(2):192-5. Epub 2015 Mar 28.

Netherlands Institute of Ecology.

Phosphate release from sediments hampers the remediation of aquatic systems from a eutrophic state. Microbial phosphatases in sediments release phosphorus during organic matter degradation. Despite the important role of phosphatase-expressing bacteria, the identity of these bacteria in sediments is largely unknown. We herein presented a culture-independent method to phylogenetically characterize phosphatase-expressing bacteria in sediments. We labeled whole-cell extracts of Baltic Sea sediments with an artificial phosphatase substrate and sorted phosphatase-expressing cells with a flow cytometer. Their phylogenetic affiliation was determined by Denaturing Gradient Gel Electrophoresis. The phosphatase-expressing bacterial community coarsely reflected the whole-cell bacterial community, with a similar dominance of Alphaproteobacteria.
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http://dx.doi.org/10.1264/jsme2.ME14074DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4462931PMC
March 2016

Ammonia-limited conditions cause of Thaumarchaeal dominance in volcanic grassland soil.

FEMS Microbiol Ecol 2015 Mar 5;91(3). Epub 2015 Feb 5.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen 6708 PB, the Netherlands Institute of Environmental Biology, University of Utrecht, 3584 CH, Utrecht, the Netherlands.

The first step of nitrification is carried out by ammonia-oxidizing bacteria (AOB) and archaea (AOA). It is largely unknown, by which mechanisms these microbes are capable of coexistence and how their respective contribution to ammonia oxidation may differ with varying soil characteristics. To determine how different levels of ammonium availability influence the extent of archaeal and bacterial contributions to ammonia oxidation, microcosm incubations with controlled ammonium levels were conducted. Net nitrification was monitored and ammonia-oxidizer communities were quantified. Additionally, the nitrification inhibitor allylthiourea (ATU) was applied to discriminate between archaeal and bacterial contributions to soil ammonia oxidation. Thaumarchaeota, which were the only ammonia oxidizers detectable at the start of the incubation, grew in all microcosms, but AOB later became detectable in ammonium amended microcosms. Low and high additions of ammonium increasingly stimulated AOB growth, while AOA were only stimulated by the low addition. Treatment with ATU had no effect on net nitrification and sizes of ammonia-oxidizing communities suggesting that the effective concentration of ATU to discriminate between archaeal and bacterial ammonia oxidation is not the same in different soils. Our results support the niche-differentiating potential of ammonium concentration for AOA and AOB, and we conclude that ammonium limitation can be a major reason for absence of detectable AOB in soil.
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http://dx.doi.org/10.1093/femsec/fiv014DOI Listing
March 2015

Cattle Manure Enhances Methanogens Diversity and Methane Emissions Compared to Swine Manure under Rice Paddy.

PLoS One 2014 10;9(12):e113593. Epub 2014 Dec 10.

Division of Applied Life Science (BK 21 Program), Gyeongsang National University, Jinju, South Korea; Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, South Korea.

Livestock manures are broadly used in agriculture to improve soil quality. However, manure application can increase the availability of organic carbon, thereby facilitating methane (CH4) production. Cattle and swine manures are expected to have different CH4 emission characteristics in rice paddy soil due to the inherent differences in composition as a result of contrasting diets and digestive physiology between the two livestock types. To compare the effect of ruminant and non-ruminant animal manure applications on CH4 emissions and methanogenic archaeal diversity during rice cultivation (June to September, 2009), fresh cattle and swine manures were applied into experimental pots at 0, 20 and 40 Mg fresh weight (FW) ha-1 in a greenhouse. Applications of manures significantly enhanced total CH4 emissions as compared to chemical fertilization, with cattle manure leading to higher emissions than swine manure. Total organic C contents in cattle (466 g kg-1) and swine (460 g kg-1) manures were of comparable results. Soil organic C (SOC) contents were also similar between the two manure treatments, but dissolved organic C (DOC) was significantly higher in cattle than swine manure. The mcrA gene copy numbers were significantly higher in cattle than swine manure. Diverse groups of methanogens which belong to Methanomicrobiaceae were detected only in cattle-manured but not in swine-manured soil. Methanogens were transferred from cattle manure to rice paddy soils through fresh excrement. In conclusion, cattle manure application can significantly increase CH4 emissions in rice paddy soil during cultivation, and its pretreatment to suppress methanogenic activity without decreasing rice productivity should be considered.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0113593PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4262209PMC
October 2017

Trait-based approaches for understanding microbial biodiversity and ecosystem functioning.

Front Microbiol 2014 27;5:251. Epub 2014 May 27.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW) Wageningen, Netherlands.

In ecology, biodiversity-ecosystem functioning (BEF) research has seen a shift in perspective from taxonomy to function in the last two decades, with successful application of trait-based approaches. This shift offers opportunities for a deeper mechanistic understanding of the role of biodiversity in maintaining multiple ecosystem processes and services. In this paper, we highlight studies that have focused on BEF of microbial communities with an emphasis on integrating trait-based approaches to microbial ecology. In doing so, we explore some of the inherent challenges and opportunities of understanding BEF using microbial systems. For example, microbial biologists characterize communities using gene phylogenies that are often unable to resolve functional traits. Additionally, experimental designs of existing microbial BEF studies are often inadequate to unravel BEF relationships. We argue that combining eco-physiological studies with contemporary molecular tools in a trait-based framework can reinforce our ability to link microbial diversity to ecosystem processes. We conclude that such trait-based approaches are a promising framework to increase the understanding of microbial BEF relationships and thus generating systematic principles in microbial ecology and more generally ecology.
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http://dx.doi.org/10.3389/fmicb.2014.00251DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4033906PMC
June 2014

Interactions between Thaumarchaea, Nitrospira and methanotrophs modulate autotrophic nitrification in volcanic grassland soil.

ISME J 2014 Dec 23;8(12):2397-410. Epub 2014 May 23.

1] Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands [2] Institute of Environmental Biology, University of Utrecht, Utrecht, The Netherlands.

Ammonium/ammonia is the sole energy substrate of ammonia oxidizers, and is also an essential nitrogen source for other microorganisms. Ammonia oxidizers therefore must compete with other soil microorganisms such as methane-oxidizing bacteria (MOB) in terrestrial ecosystems when ammonium concentrations are limiting. Here we report on the interactions between nitrifying communities dominated by ammonia-oxidizing archaea (AOA) and Nitrospira-like nitrite-oxidizing bacteria (NOB), and communities of MOB in controlled microcosm experiments with two levels of ammonium and methane availability. We observed strong stimulatory effects of elevated ammonium concentration on the processes of nitrification and methane oxidation as well as on the abundances of autotrophically growing nitrifiers. However, the key players in nitrification and methane oxidation, identified by stable-isotope labeling using (13)CO2 and (13)CH4, were the same under both ammonium levels, namely type 1.1a AOA, sublineage I and II Nitrospira-like NOB and Methylomicrobium-/Methylosarcina-like MOB, respectively. Ammonia-oxidizing bacteria were nearly absent, and ammonia oxidation could almost exclusively be attributed to AOA. Interestingly, although AOA functional gene abundance increased 10-fold during incubation, there was very limited evidence of autotrophic growth, suggesting a partly mixotrophic lifestyle. Furthermore, autotrophic growth of AOA and NOB was inhibited by active MOB at both ammonium levels. Our results suggest the existence of a previously overlooked competition for nitrogen between nitrifiers and methane oxidizers in soil, thus linking two of the most important biogeochemical cycles in nature.
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http://dx.doi.org/10.1038/ismej.2014.81DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4260704PMC
December 2014

Effect of redox conditions on bacterial community structure in Baltic Sea sediments with contrasting phosphorus fluxes.

PLoS One 2014 25;9(3):e92401. Epub 2014 Mar 25.

Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands; Institute of Environmental Biology, Science Faculty, Utrecht University, Utrecht, The Netherlands.

Phosphorus release from sediments can exacerbate the effect of eutrophication in coastal marine ecosystems. The flux of phosphorus from marine sediments to the overlying water is highly dependent on the redox conditions at the sediment-water interface. Bacteria are key players in the biological processes that release or retain phosphorus in marine sediments. To gain more insight in the role of bacteria in phosphorus release from sediments, we assessed the effect of redox conditions on the structure of bacterial communities. To do so, we incubated surface sediments from four sampling sites in the Baltic Sea under oxic and anoxic conditions and analyzed the fingerprints of the bacterial community structures in these incubations and the original sediments. This paper describes the effects of redox conditions, sampling station, and sample type (DNA, RNA, or whole-cell sample) on bacterial community structure in sediments. Redox conditions explained only 5% of the variance in community structure, and bacterial communities from contrasting redox conditions showed considerable overlap. We conclude that benthic bacterial communities cannot be classified as being typical for oxic or anoxic conditions based on community structure fingerprints. Our results suggest that the overall structure of the benthic bacterial community has only a limited impact on benthic phosphate fluxes in the Baltic Sea.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0092401PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3965429PMC
January 2015

Remarkable recovery and colonization behaviour of methane oxidizing bacteria in soil after disturbance is controlled by methane source only.

Microb Ecol 2014 Aug;68(2):259-70

Little is understood about the relationship between microbial assemblage history, the composition and function of specific functional guilds and the ecosystem functions they provide. To learn more about this relationship we used methane oxidizing bacteria (MOB) as model organisms and performed soil microcosm experiments comprised of identical soil substrates, hosting distinct overall microbial diversities(i.e., full, reduced and zero total microbial and MOB diversities). After inoculation with undisturbed soil, the recovery of MOB activity, MOB diversity and total bacterial diversity were followed over 3 months by methane oxidation potential measurements and analyses targeting pmoA and 16S rRNA genes. Measurement of methane oxidation potential demonstrated different recovery rates across the different treatments. Despite different starting microbial diversities, the recovery and succession of the MOB communities followed a similar pattern across the different treatment microcosms. In this study we found that edaphic parameters were the dominant factor shaping microbial communities over time and that the starting microbial community played only a minor role in shaping MOB microbial community.
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http://dx.doi.org/10.1007/s00248-014-0402-9DOI Listing
August 2014

Microbial minorities modulate methane consumption through niche partitioning.

ISME J 2013 Nov 20;7(11):2214-28. Epub 2013 Jun 20.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.

Microbes catalyze all major geochemical cycles on earth. However, the role of microbial traits and community composition in biogeochemical cycles is still poorly understood mainly due to the inability to assess the community members that are actually performing biogeochemical conversions in complex environmental samples. Here we applied a polyphasic approach to assess the role of microbial community composition in modulating methane emission from a riparian floodplain. We show that the dynamics and intensity of methane consumption in riparian wetlands coincide with relative abundance and activity of specific subgroups of methane-oxidizing bacteria (MOB), which can be considered as a minor component of the microbial community in this ecosystem. Microarray-based community composition analyses demonstrated linear relationships of MOB diversity parameters and in vitro methane consumption. Incubations using intact cores in combination with stable isotope labeling of lipids and proteins corroborated the correlative evidence from in vitro incubations demonstrating γ-proteobacterial MOB subgroups to be responsible for methane oxidation. The results obtained within the riparian flooding gradient collectively demonstrate that niche partitioning of MOB within a community comprised of a very limited amount of active species modulates methane consumption and emission from this wetland. The implications of the results obtained for biodiversity-ecosystem functioning are discussed with special reference to the role of spatial and temporal heterogeneity and functional redundancy.
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http://dx.doi.org/10.1038/ismej.2013.99DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3806271PMC
November 2013

Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies.

Environ Microbiol Rep 2013 Jun 13;5(3):335-45. Epub 2012 Aug 13.

Laboratory of Microbial Ecology and Technology (LabMET), Faculty of Bioscience Engineering, Coupure Links 653, B-9000 Ghent, Belgium.

Methane-oxidizing bacteria (MOB) possess the ability to use methane for energy generation and growth, thereby, providing a key ecosystem service that is highly relevant to the regulation of the global climate. MOB subgroups have different responses to key environmental controls, reflecting on their functional traits. Their unique features (C1-metabolism, unique lipids and congruence between the 16S rRNA and pmoA gene phylogeny) have facilitated numerous environmental studies, which in combination with the availability of cultured representatives, yield the most comprehensive ecological picture of any known microbial functional guild. Here, we focus on the broad MOB subgroups (type I and type II MOB), and aim to conceptualize MOB functional traits and observational characteristics derived primarily from these environmental studies to be interpreted as microbial life strategies. We focus on the functional traits, and the conditions under which these traits will render different MOB subgroups a selective advantage. We hypothesize that type I and type II MOB generally have distinct life strategies, enabling them to predominate under different conditions and maintain functionality. The ecological characteristics implicated in their adopted life strategies are discussed, and incorporated into the Competitor-Stress tolerator-Ruderal functional classification framework as put forward for plant communities. In this context, type I MOB can broadly be classified as competitor-ruderal while type II MOB fit more within the stress tolerator categories. Finally, we provide an outlook on MOB applications by exemplifying two approaches where their inferred life strategies could be exploited thereby, putting MOB into the context of microbial resource management.
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http://dx.doi.org/10.1111/j.1758-2229.2012.00370.xDOI Listing
June 2013