Combining metagenomics with metaproteomics and stable isotope probing reveals metabolic pathways used by a naturally occurring marine methylotroph

Grob, Carolina; Taubert, Martin; Howat, Alexandra M.; Burns, Oliver J.; Dixon, Joanna L.; Richnow, Hans H.; Jehmlich, Nico; Bergen, Martin von; Chen, Yin; Murrell, J. Colin

doi:10.1111/1462-2920.12935

Cited by 52 publications

(36 citation statements)

References 68 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In addition to testing the impacts of timber harvesting, we sought to expand general knowledge of cellulolytic populations in forest soils and to characterize the cellulolytic potential of mineral layer soils for the first time. We provide one of the first examples of SIP coupled to shotgun metagenomics (others include Grob et al, 2015), for which we describe the effective enrichment and recovery of metagenome-assembled genomes (MAGs) from novel, uncultured cellulolytic taxa.…”

Section: Introductionmentioning

confidence: 99%

Long-Term Enrichment of Stress-Tolerant Cellulolytic Soil Populations following Timber Harvesting Evidenced by Multi-Omic Stable Isotope Probing

et al. 2017

View full text Add to dashboard Cite

Soil management is vital for maintaining the productivity of commercial forests, yet the long-term impact of timber harvesting on soil microbial communities remains largely a matter of conjecture. Decomposition of plant biomass, comprised mainly of lignocellulose, has a broad impact on nutrient cycling, microbial activity and physicochemical characteristics of soil. At “Long-term Soil Productivity Study” sites in California dominated by Ponderosa pine, we tested whether clear-cut timber harvesting, accompanied by varying degrees of organic matter (OM) removal, affected the activity and structure of the cellulose-degrading microbial populations 16 years after harvesting. Using a variety of experimental approaches, including stable isotope probing with 13C-labeled cellulose in soil microcosms, we demonstrated that harvesting led to a decrease in net respiration and cellulolytic activity. The decrease in cellulolytic activity was associated with an increased relative abundance of thermophilic, cellulolytic fungi (Chaetomiaceae), coupled with a decreased relative abundance of cellulolytic bacteria, particularly members of Opitutaceae, Caulobacter, and Streptomycetaceae. In general, harvesting led to an increase in stress-tolerant taxa (i.e., also non-cellulolytic taxa), though our results indicated that OM retention mitigated population shifts via buffering against abiotic changes. Stable-isotope probing improved shotgun metagenome assembly by 20-fold and enabled the recovery of 10 metagenome-assembled genomes of cellulolytic bacteria and fungi. Our study demonstrates the putative cellulolytic activity of a number of uncultured taxa and highlights the mineral soil layer as a reservoir of uncharacterized diversity of cellulose-degraders. It also and contributes to a growing body of research showing persistent changes in microbial community structure in the decades following forest harvesting.

show abstract

Section: Introductionmentioning

confidence: 99%

Long-Term Enrichment of Stress-Tolerant Cellulolytic Soil Populations following Timber Harvesting Evidenced by Multi-Omic Stable Isotope Probing

et al. 2017

View full text Add to dashboard Cite

show abstract

“…For Methylophaga sp., key enzymes of the ribulose monophosphate cycle for carbon assimilation and enzymes involved in the tetrahydromethanopterin‐ and tetrahydrofolate‐dependent oxidation/reduction of C1 groups were detected. This resembles the metabolism of the closely related Methylophaga thiooxydans strain L4 during growth on methanol, as previously described (Grob et al ., ). Methylophaga spp.…”

Section: Resultsmentioning

confidence: 98%

“…Expression of functional genes involved in methylamine degradation. Shown are the gene clusters encoding proteins of the gammaglutamyl methylamide pathway from the genomes sequenced in this study, related to Gammaproteobacterium IMCC2047 and Leisingera , and from the published genomes of Methylophaga thiooxydans strain L4 1 (Grob et al , Environ Microbiol 17(10):4007‐4018) and Candidatus Pelagibacter ubique HTCC1062 2 (Giovannoni et al , Science 309(5738):1242‐1245). The gene cluster encoding proteins of the methylamine dehydrogenase pathway of Methylophaga thiooxydans is also shown.…”

mentioning

confidence: 99%

Methylamine as a nitrogen source for microorganisms from a coastal marine environment

Taubert

Grob

Howat

et al. 2017

Environmental Microbiology

Self Cite

View full text Add to dashboard Cite

Nitrogen is a key limiting resource for biomass production in the marine environment. Methylated amines, released from the degradation of osmolytes, could provide a nitrogen source for marine microbes. Thus far, studies in aquatic habitats on the utilization of methylamine, the simplest methylated amine, have mainly focussed on the fate of the carbon from this compound. Various groups of methylotrophs, microorganisms that can grow on one-carbon compounds, use methylamine as a carbon source. Non-methylotrophic microorganisms may also utilize methylamine as a nitrogen source, but little is known about their diversity, especially in the marine environment. In this proof-of-concept study, stable isotope probing (SIP) was used to identify microorganisms from a coastal environment that assimilate nitrogen from methylamine. SIP experiments using N methylamine combined with metagenomics and metaproteomics facilitated identification of active methylamine-utilizing Alpha- and Gammaproteobacteria. The draft genomes of two methylamine utilizers were obtained and their metabolism with respect to methylamine was examined. Both bacteria identified in these SIP experiments used the γ-glutamyl-methylamide pathway, found in both methylotrophs and non-methylotrophs, to metabolize methylamine. The utilization of N methylamine also led to the release of N ammonium that was used as nitrogen source by other microorganisms not directly using methylamine.

show abstract

“…The study of microbial communities from nutrient-enriched coastal systems shows the large subunit of methanol dehydrogenase from the OM43 clade in almost all the samples [47]. In a proof-of-concept experiment, the RuMP cycle is regarded as the main carbon assimilation pathway in the Methylophaga -like bacterium [49]. Moreover, hexulose-6-phosphate synthase, the key enzyme of the RuMP pathway of OM43, is also detected in all Atlantic Ocean samples.…”

Section: Microbial Community Proteomics In Various Environmentsmentioning

confidence: 99%

Environmental Microbial Community Proteomics: Status, Challenges and Perspectives

Wang

Kong

Xie

2016

IJMS

View full text Add to dashboard Cite

Microbial community proteomics, also termed metaproteomics, is an emerging field within the area of microbiology, which studies the entire protein complement recovered directly from a complex environmental microbial community at a given point in time. Although it is still in its infancy, microbial community proteomics has shown its powerful potential in exploring microbial diversity, metabolic potential, ecological function and microbe-environment interactions. In this paper, we review recent advances achieved in microbial community proteomics conducted in diverse environments, such as marine and freshwater, sediment and soil, activated sludge, acid mine drainage biofilms and symbiotic communities. The challenges facing microbial community proteomics are also discussed, and we believe that microbial community proteomics will greatly enhance our understanding of the microbial world and its interactions with the environment.

show abstract

Combining metagenomics with metaproteomics and stable isotope probing reveals metabolic pathways used by a naturally occurring marine methylotroph

Cited by 52 publications

References 68 publications

Long-Term Enrichment of Stress-Tolerant Cellulolytic Soil Populations following Timber Harvesting Evidenced by Multi-Omic Stable Isotope Probing

Long-Term Enrichment of Stress-Tolerant Cellulolytic Soil Populations following Timber Harvesting Evidenced by Multi-Omic Stable Isotope Probing

Methylamine as a nitrogen source for microorganisms from a coastal marine environment

Environmental Microbial Community Proteomics: Status, Challenges and Perspectives

Contact Info

Product

Resources

About