Editorial on the Research Topic: The Impact of Microorganisms on Consumption of Atmospheric Trace Gase

Horn, Marcus A.

Knief, Claudia

Kolb, Steffen

Murrell, J. Colin

Frontiers in Microbiology

Steffen Kolb

Marcus A. Horn

J. Colin Murrell

Claudia Knief

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Editorial: The Impact of Microorganisms on Consumption of Atmospheric Trace Gases

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EDITORIALpublished: 28 September 2017doi: 10.3389/fmicb.2017.01856Frontiers in Microbiology | www.frontiersin.org 1 September 2017 | Volume 8 | Article 1856Edited by:Paul Bodelier,Netherlands Institute of Ecology(NIOO-KNAW), NetherlandsReviewed by:Svetlana N. Dedysh,Winogradsky Institute of Microbiology(RAS), Russia*Correspondence:Steffen Kolbkolb@zalf.deSpecialty section:This article was submitted toTerrestrial Microbiology,a section of the journalFrontiers in MicrobiologyReceived: 17 August 2017Accepted: 11 September 2017Published: 28 September 2017Citation:Kolb S, Horn MA, Murrell JC andKnief C (2017) Editorial: The Impact ofMicroorganisms on Consumption ofAtmospheric Trace Gases.Front. Microbiol. 8:1856.doi: 10.3389/fmicb.2017.01856Editorial: The Impact ofMicroorganisms on Consumption ofAtmospheric Trace GasesSteffen Kolb 1*, Marcus A. Horn 2, J. Colin Murrell 3 and Claudia Knief 41 Leibniz Zentrum für Agrarlandschaftsforschung e.V., Institute Landschaftsbiogeochemie, Müncheberg, Germany,2 Bodenmikrobiologie, Institut für Mikrobiologie, Leibniz-Universität Hannover, Hannover, Germany, 3 School of EnvironmentalSciences, University of East Anglia, Norwich, United Kingdom, 4Molekularbiologie der Rhizosphäre, Institut fürNutzpflanzenwissenschaften und Ressourcenschutz, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, GermanyKeywords: methane, methanotroph, nitrous oxide, denitrification, volatile organic compounds, carbon monoxide,phyllosphereEditorial on the Research TopicThe Impact of Microorganisms on Consumption of Atmospheric Trace GasesGases with a mixing ratio of <1% in the atmosphere are considered as trace gases. Several ofthese trace gases originate from biological processes in marine and terrestrial ecosystems and areof relevance for the climate as they contribute to global warming, to the troposphere’s chemicalreactive system that builds the ozone layer, or they impact on the stability of aerosols, greenhouse,and pollutant gases (Conrad, 2009; Arneth et al., 2010; Penuelas and Staudt, 2010). These gasesinclude methane (CH4), a multitude of volatile organic compounds of biogenic origin (bVOCs)and inorganic gases such as nitrogen oxides or ozone (Conrad, 2009; Hewitt et al., 2011; Peñuelaset al., 2014; Fowler et al., 2016). The important role of microorganisms for trace gas cycling hasbeen intensively studied for the greenhouse gases nitrous oxide (N2O) and methane (CH4), but isless well-understood for organisms that metabolize H2, carbon monoxide (CO), or bVOCs. Thestudies compiled in this Research Topic reflect this very well. While a number of articles focus onN2O and CH4 cycling or CO oxidation, only a few articles address conversion processes of bVOCs(Dixon et al.; Nadalig et al.). The Research Topic is complemented by three review articles aboutthe consumption of CH4 and monoterpenes, as well as the role of the phyllosphere as a particularhabitat for trace gas-consuming microorganisms, and points out future research directions in thefield (Marmulla and Harder; Bringel and Couee; Knief).Articles in this research topic on N2O cycling are related to terrestrial environments anddenitrification. Soil N2O emissions result from different biological processes with nitrification anddenitrification being the most important ones. Denitrifiers are facultative aerobic microorganismsthat reduce nitrate (NO−3 ) or nitrite (NO−2 ) to the gaseous products nitric oxide (NO), nitrousoxide (N2O), or dinitrogen (N2) under oxygen-limited conditions. Various environmental factorshave been identified that affect the composition, abundance, and activity of these microbial groups(reviewed in Braker and Conrad, 2011). The study of Brenzinger et al. evaluates changes onthe denitrifier microbiota and gene expression upon pH shifts. Their observation of changes ingene expression of specific taxa demonstrates that functional redundancy of the soil microbiomeis important to maintain denitrification upon acidification. Functional redundancy and processpartitioning among NO−3 - and N2O-reducing denitrifiers can also explain the findings that insitu N2O fluxes were largely unaffected upon manipulations of the water table in a wetland,although an increase in N2O reduction activity was observed upon flooding (Palmer et al.). Incontrast, land-use change of an agroforest system to an open area converted a cork oak wood fromKolb et al. Editorial: Microbial Trace Gase Consumptiona N2O source to a sink (Shvaleva et al.). This change wasnot reflected in the abundance of the denitrifier gene nosZ.All of these studies demonstrate that the underlying microbialprocesses that control N2O fluxes are complex and require acomprehensive analysis of all the different microbial groupsthat may be involved. Moreover, information about microbiomecomposition needs to be complemented by data on taxonabundance, activity, and ecophysiology of isolates in order toobtain an understanding of the mechanisms underpinning theobservable net ecosystem N2O fluxes.To better assess the biotic mechanisms driving N2O fluxes,in vitro analyses of pure cultures are helpful, as exemplified bytwo studies in this Research topic. Bueno et al. revealed thatthe well-known soil microorganism Ensifer meliloti strain 1021displays a phenotype that enables it to function as a sink for N2Odue to anaerobic N2O respiration. Remarkably, it appears thatthis strain is not able to grow via NO−3 respiration, although itcan express all genes encoding a complete set of denitrificationenzymes. More work is needed to elucidate this peculiarity.Kits et al. studied denitrification activity in the methanotrophMethylomicrobium album BG8. Although methanotrophs areconsidered to be the major biological sink for CH4 in soil, someof them also form N2O through denitrification under hypoxicconditions. The authors prove in their study that M. albumBG8 carries out denitrification using nitrite as electron acceptorwhile oxidizing a range of different one- and even two-carboncompounds, i.e., ethane and ethanol.The microbial ecology of methanotrophs has been studied fordecades, due to the importance of CH4 as greenhouse gas. Thishas substantially increased knowledge on their ecophysiologyand environmental distribution, as summarized in the review byKnief. Methanotrophic communities are often analyzed based onthe marker gene pmoA, encoding a subunit of the membrane-bound methane monooxygenase. The extensive sequencing ofpmoA has led to the identification of a number of new taxa.Based on this information, the occurrence of the different taxain diverse ecosystems was analyzed within a meta-analysis, thusproviding new knowledge about habitat preferences of specificmethanotroph taxa. Some methanotroph taxa were identified asspecialists, occurring only in specific ecosystems, while othergenera appear to be generalists (Knief). Rather specific habitatpreferences have for example been suggested for a groupof uncultured atmospheric CH4-consuming methanotrophs(termed USCα), with upland soils and especially forest soilsbeing the preferred habitat (Kolb, 2009). The conversion of anAmazonian forest into a manioc (cassava) plantation resulted indrastically decreased abundance of this group of methanotrophsconcomitant with the CH4 sink activity (Lima et al.). Remarkably,this response was only observed in one of the two soils studied.In an Amazonian Dark Earth (syn. terra preta) soil, USCα wasstill abundant and CH4 uptake rates remained high 5 yearsafter deforestation and manioc cultivation. The causes for thisdifference are unclear and need further investigation.Research on the biological cycling of other one-carbon VOCssuch as CO or chloromethane has attracted less attention untilnow, despite the fact that these gases play a crucial role inatmospheric chemistry and impact on the global climate (Danieland Solomon, 1998; Harper, 2000). The Research Topic includesthree studies addressing CO oxidation, which demonstrate nicelythe different experimental approaches that can be taken to studya specific functional guild in the environment. Lynch et al.studied trace gas consumers in dry high-elevation mineral soilsoriginating from volcanic deposits in the Atacama Desert viaa metagenomic analysis of the soil microbiome, and minedfor genes and pathways known to be involved in trace gasconversion. The authors were able to reconstruct the genome ofthe dominant taxon, Pseudonocardia sp., and revealed geneticpotential of this organism for hydrogen (H2), CO, and somefurther one-carbon compounds oxidation. In the study by Quizaet al., aerobic CO oxidizing microorganisms were specificallydetected by targeting a functional gene marker, coxL, encodingthe large subunit of the CO-dehydrogenase. Highest activities,along with the detection of distinct aerobic CO oxidizers, wereobserved in a deciduous forest soil, compared to an adjacentafforested larch plantation and a maize field. Brady et al.applied stable isotope probing (SIP) in combination with 16SrRNA gene sequencing. SIP is a valuable method to specificallyidentify the metabolically active microbiome members butrequires 13CO2 controls to distinguish between CO- andCO2-assimilating microorganisms. Brady et al. identified novelmembers of Firmicutes as autotrophic CO consumers in oxygen-limited geothermal springs using this experimental approach.The fact that heterotrophic carboxydotrophs, which use COonly as an energy source, will be missed by SIP highlightsthe need for the application of complementary approachesto comprehensively assess the role of CO consumers in theenvironment.Chloromethane is a bVOC, and the most abundanthalogenated compound in the atmosphere. The onlyknown aerobic pathway for chloromethane oxidation is thecmu pathway, which has been well-investigated in aerobicAlphaproteobacteria (Nadalig et al.). Based on a genomic survey,Nadalig et al. show that the cmu pathway occurs in severalother bacterial taxa, including obligate anaerobes. Interestingly,the authors found that the genome of the aerobe Leisingeriamethylhalidivorans, i.e., a known chloromethane degrader,does not have the cmu pathway. Moreover, the authors provedthat L. methylhalidivorans has diverging isotopic signatures of13C and 2H when assimilating chloromethane compared toother alphaproteobacterial cmu-containing strains, suggestingthe existence of a hitherto unknown pathway. This studydemonstrates the limited knowledge we currently have aboutmicrobial bVOC metabolism. Another example is given bythe review of Marmulla and Harder who provide an overviewon the complex biochemistry and pathways of monoterpenedegradation in microorganisms and conclude that thesepathways need to be studied in more detail in the future.Considering the multitude of monoterpenes present in nature,it is evident that more research is needed. Knowledge about thebiochemistry, the genetic makeup of the metabolic pathways, andtheir distribution among microorganisms is an indispensableprerequisite to perform environmental studies with the aim toimprove our understanding of how microbiomes control tracegas fluxes.Frontiers in Microbiology | www.frontiersin.org 2 September 2017 | Volume 8 | Article 1856Kolb et al. Editorial: Microbial Trace Gase ConsumptionThe aforementioned studies of the Research Topic highlightthat our current knowledge about the identity of microorganismsinvolved in the production or consumption of trace gasesand, in particular bVOCs, is limited. For most bVOCs, theimpact of microbial consumption on net fluxes between soilor marine ecosystems and the atmosphere is not clear todate. The study of Dixon et al. is one rare example onmicrobial acetone oxidation in marine waters with seasonalresolution and estimates the quantitative proportion of acetonecarbon consumption compared to other bVOCs. Remarkably,the data suggest the existence of an unrecognized productionmechanism for acetone during the winter. Besides soils andaquatic habitats, another major habitat for trace gas metabolizingmicroorganisms is the plant leaf surface, often referred to asthe phyllosphere. Considering that plants are major producersof bVOCs (Penuelas and Staudt, 2010), their leaves representan important interface to the atmosphere and are colonizedby microorganisms. Bringel and Couee emphasize in theirreview the need to study this aspect in more detail. Theauthors summarize current knowledge about phyllospheremicroorganisms metabolizing bVOCs, which is largely limited toone-carbon compounds.Knowledge about microbial consumption of bVOCs is farfrom being compared to knowledge on microbial consumptionof CH4 or N2O. This includes the quantitative relevance ofmicrobial activities at the ecosystem level and globally, theidentities of trace gas degrading microorganisms, the analysis oftheir degradation pathways, as well as the physiological traitsthat finally determining the activity of these microbes in situ.Thus, the research field of microbial trace gas consumption canbe considered to be still in its infancy and necessitates futureresearch to better quantitatively consider microbial trace gasconversions at an ecosystem level, e.g., in upcoming modelingefforts (Graham et al., 2016).AUTHOR CONTRIBUTIONSAll authors were involved in the set-up and design of thisResearch Topic. SK and CK wrote this editorial, MH and JMprovided valuable comments.REFERENCESArneth, A., Sitch, S., Bondeau, A., Butterbach-Bahl, K., Foster, P., Gedney, N.,et al. (2010). From biota to chemistry and climate: towards a comprehensivedescription of trace gas exchange between the biosphere and atmosphere.Biogeosciences 7, 121–149. doi: 10.5194/bg-7-121-2010Braker, G., and Conrad, R. (2011). Diversity, structure, and size of N2O-producing microbial communities in soils - what matters for their functioning?Adv. Appl. Microbiol. 75, 33–70. doi: 10.1016/B978-0-12-387046-9.00002-5Conrad, R. (2009). The global methane cycle: recent advances in understandingthe microbial processes involved. Environ. Microbiol. Rep. 1, 285–292.doi: 10.1111/j.1758-2229.2009.00038.xDaniel, J. S., and Solomon, S. (1998). On the climate forcing of carbonmonoxide. J. Geophys. Res. Atmos. 103, 13249–13260. doi: 10.1029/98JD00822Fowler, D., Coyle, M., Skiba, U., Sutton, M. A., Cape, J. N., Reis, S., et al. (2016).The global nitrogen cycle in the twenty-first century. Philos. Trans. R. Soc. B368:20130164. doi: 10.1098/rstb.2013.0164Graham, E. B., Knelman, J. E., Schindlbacher, A., Siciliano, S., Breulmann, M.,Yannarell, A., et al. (2016). Microbes as engines of ecosystem function: whendoes community structure enhance predictions of ecosystem processes? Front.Microbiol. 7:214. doi: 10.3389/fmicb.2016.00214Harper, D. B. (2000). The global chloromethane cycle: biosynthesis, biodegradationand metabolic role. Nat. Prod. Rep. 17, 337–348. doi: 10.1039/a809400dHewitt, C. N., Karl, T., Langford, B., Owen, S. M., and Possell, M. (2011).Quantification of VOC emission rates from the biosphere. Trace Trends Anal.Chem. 30, 937–944. doi: 10.1016/j.trac.2011.03.008Kolb, S. (2009). The quest for atmospheric methane oxidizers in forest soils.Environ. Microbiol. Rep. 1, 336–346. doi: 10.1111/j.1758-2229.2009.00047.xPenuelas, J., and Staudt, M. (2010). BVOCs and global change. Trends Plant Sci.15, 133–144. doi: 10.1016/j.tplants.2009.12.005Peñuelas, J., Asensio, D., Tholl, D., Wenke, K., Rosenkranz, M., Piechulla, B.,et al. (2014). Biogenic volatile emissions from the soil. Plant Cell Environ. 37,1866–1891. doi: 10.1111/pce.12340Conflict of Interest Statement: The authors declare that the research wasconducted in the absence of any commercial or financial relationships that couldbe construed as a potential conflict of interest.Copyright © 2017 Kolb, Horn, Murrell and Knief. This is an open-access articledistributed under the terms of the Creative Commons Attribution License (CC BY).The use, distribution or reproduction in other forums is permitted, provided theoriginal author(s) or licensor are credited and that the original publication in thisjournal is cited, in accordance with accepted academic practice. No use, distributionor reproduction is permitted which does not comply with these terms.Frontiers in Microbiology | www.frontiersin.org 3 September 2017 | Volume 8 | Article 1856

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