Tree phyllospheres are a habitat for diverse populations of CO-oxidizing bacteria.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
revised:
21
07
2021
received:
14
04
2021
accepted:
08
09
2021
pubmed:
16
9
2021
medline:
18
3
2022
entrez:
15
9
2021
Statut:
ppublish
Résumé
Carbon monoxide (CO) is both a ubiquitous atmospheric trace gas and an air pollutant. While aerobic CO-degrading microorganisms in soils and oceans are estimated to remove ~370 Tg of CO per year, the presence of CO-degrading microorganisms in above-ground habitats, such as the phyllosphere, and their potential role in CO cycling remains unknown. CO-degradation by leaf washes of two common British trees, Ilex aquifolium and Crataegus monogyna, demonstrated CO uptake in all samples investigated. Based on the analyses of taxonomic and functional genes, diverse communities of candidate CO-oxidizing taxa were identified, including members of Rhizobiales and Burkholderiales which were abundant in the phyllosphere at the time of sampling. Based on predicted genomes of phyllosphere community members, an estimated 21% of phyllosphere bacteria contained CoxL, the large subunit of CO-dehydrogenase. In support of this, data mining of publicly available phyllosphere metagenomes for genes encoding CO-dehydrogenase subunits demonstrated that, on average, 25% of phyllosphere bacteria contained CO-dehydrogenase gene homologues. A CO-oxidizing Phyllobacteriaceae strain was also isolated from phyllosphere samples which contains genes encoding both CO-dehydrogenase as well as a ribulose-1,5-bisphosphate carboxylase-oxygenase. These results suggest that the phyllosphere supports diverse and potentially abundant CO-oxidizing bacteria, which are a potential sink for atmospheric CO.
Identifiants
pubmed: 34523801
doi: 10.1111/1462-2920.15770
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
6309-6327Informations de copyright
© 2021 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Abanda-Nkpwatt, D., Müsch, M., Tschiersch, J., Boettner, M., and Schwab, W. (2006) Molecular interaction between Methylobacterium extorquens and seedlings: growth promotion, methanol consumption, and localization of the methanol emission site. J Exp Bot 57: 4025-4032.
Atamna-Ismaeel, N., Finkel, O.M., Glaser, F., Sharon, I., Schneider, R., Post, A.F., et al. (2011) Microbial rhodopsins on leaf surfaces of terrestrial plants. Environ Microbiol 14: 140-146.
Aziz, R.K., Bartels, D., Best, A.A., DeJongh, M., Disz, T., Edwards, R.A., et al. (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9: 1-15.
Badr, O., and Probert, S. (1994) Carbon monoxide concentration in the Earth's atmosphere. Appl Energy 49: 99-143.
Badr, O., and Probert, S. (1995) Sinks and environmental impacts for atmospheric carbon monoxide. Appl Energy 50: 339-372.
Bankevich, A., Nurk, S., Antipov, D., Gurevich, A.A., Dvorkin, M., Kulikov, A.S., et al. (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19: 455-477.
Bay, S.K., Dong, X., Bradley, J.A., Leung, P.M., Grinter, R., Jirapanjawat, T., et al. (2021) Trace gas oxidizers are widespread and active members of soil microbial communities. Nat Microbiol 6: 246-256.
Blighe, K. (2019) EnhancedVolcano: publication-ready volcano plots with enhanced colouring and labeling. R package version 10.
Bolger, A.M., Lohse, M., and Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120.
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Huntley, J., Fierer, N., et al. (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6: 1621-1624.
Carrión, O., Gibson, L., Elias, D.M., McNamara, N.P., van Alen, T.A., Op den Camp, H.J., et al. (2020) Diversity of isoprene-degrading bacteria in phyllosphere and soil communities from a high isoprene-emitting environment: a Malaysian oil palm plantation. Microbiome 8: 1-13.
Chen, I.M.A., Chu, K., Palaniappan, K., Pillay, M., Ratner, A., Huang, J.H., et al. (2019) IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes. Nucleic Acids Res 47: D666-D677.
Clarke, K., and Gorley, R. (2005) PRIMER: Getting Started with v6. Plymouth, UK: PRIMER-E Ltd.
Conte, L., Szopa, S., Seferian, R., and Bopp, L. (2019) The oceanic cycle of carbon monoxide and its emissions to the atmosphere. Biogeosciences 16: 881-902.
Cordero, P.R., Bayly, K., Leung, P.M., Huang, C., Islam, Z.F., Schittenhelm, R.B., et al. (2019) Atmospheric carbon monoxide oxidation is a widespread mechanism supporting microbial survival. ISME J 13: 2868-2881.
Crombie, A.T., Larke-Mejia, N.L., Emery, H., Dawson, R., Pratscher, J., Murphy, G.P., et al. (2018) Poplar phyllosphere harbors disparate isoprene-degrading bacteria. Proc Natl Acad Sci USA 115: 13081-13086.
Cunliffe, M. (2011) Correlating carbon monoxide oxidation with cox genes in the abundant marine Roseobacter clade. ISME J 5: 685-691.
Daniel, J.S., and Solomon, S. (1998) On the climate forcing of carbon monoxide. J Geophys Res-Atmos 103: 13249-13260.
DEFRA. (2014) Air Pollution in the UK 2014. Department for Environment, Food and Rural Affairs, [Online]. URL https://uk-air.defra.gov.uk/library/annualreport/viewonline?year=2014_issue_1#report_pdf.
Delmotte, N., Knief, C., Chaffron, S., Innerebner, G., Roschitzki, B., Schlapbach, R., et al. (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci USA 106: 16428-16433.
Dixon, P. (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14: 927-930.
Douglas, G.M., Maffei, V.J., Zaneveld, J., Yurgel, S.N., Brown, J.R., Taylor, C.M., et al. (2019) PICRUSt2: an improved and extensible approach for metagenome inference. BioRxiv 672295. https://doi.org/10.1101/672295
Dwivedi, V.D., Arora, S., Kumar, A., and Mishra, S.K. (2013) Computational analysis of xanthine dehydrogenase enzyme from different source organisms. Netw Model Anal Health Inform Bioinform 2: 185-189.
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
Edgar, R.C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
Felsenstein, J. (1985) Confidence limits on phylogenies - an approach using the bootstrap. Evolution 39: 783-791.
Hardy, K.R., and King, G.M. (2001) Enrichment of high-affinity CO oxidizers in Maine forest soil. Appl Environ Microbiol 67: 3671-3676.
Hernández, M., Vera-Gargallo, B., Calabi-Floody, M., King, G.M., Conrad, R., and Tebbe, C.C. (2020) Reconstructing genomes of carbon monoxide oxidisers in volcanic deposits including members of the class Ktedonobacteria. Microorganisms 8: 1880.
Hogendoorn, C., Pol, A., Picone, N., Cremers, G., van Alen, T.A., Gagliano, A.L., et al. (2020) Hydrogen and carbon monoxide-utilizing Kyrpidia spormannii species from Pantelleria Island, Italy. Front Microbiol 11(951): 1-13.
Imperato, V., Kowalkowski, L., Portillo-Estrada, M., Gawronski, S.W., Vangronsveld, J., and Thijs, S. (2019) Characterisation of the Carpinus betulus L phyllomicrobiome in urban and forest areas. Front Microbiol 10(1110): 1-16.
Jindachot, W., Treesubsuntorn, C., and Thiravetyan, P. (2018) Effect of individual/co-culture of native Phyllosphere organisms to enhance Dracaena sanderiana for benzene phytoremediation. Water Air Soil Pollut 229: 80.
Johnson, M., Zaretskaya, I., Raytselis, Y., Merezhuk, Y., McGinnis, S., and Madden, T.L. (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36: W5-W9.
Kanagawa, T., Dazai, M., and Fukuoka, S. (1982) Degradation of O,O-dimethyl phosphorodithioate by Thiobacillus-thioparus TK-1 and Pseudomonas AK-2. Agric Biol Chem 46: 2571-2578.
Keegan, K.P., Glass, E.M., and Meyer, F. (2016) MG-RAST, a metagenomics service for analysis of microbial community structure and function. In F. Martin & S. Uroz (Eds), Microb Environ Genom (MEG) (Vol. 1399, pp. 207-233). Berlin, Germany: Springer.
Kembel, S.W., and Mueller, R.C. (2014) Plant traits and taxonomy drive host associations in tropical phyllosphere fungal communities. Botany 92: 303-311.
Kembel, S.W., O'Connor, T.K., Arnold, H.K., Hubbell, S.P., Wright, S.J., and Green, J.L. (2014) Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proc Natl Acad Sci USA 111: 13715-13720.
Khalil, M., and Rasmussen, R. (1984) Carbon monoxide in the earth's atmosphere: increasing trend. Science 224: 54-56.
Khalil, M.A.K., and Rasmussen, R.A. (1994) Global decrease in atmospheric carbon-monoxide concentration. Nature 370: 639-641.
King, G.A. (2003) Molecular and culture-based analyses of aerobic carbon monoxide oxidizer diversity. Appl Environ Microbiol 69: 7257-7265.
King, G.M. (1999) Attributes of atmospheric carbon monoxide oxidation by Maine forest soils. Appl Environ Microbiol 65: 5257-5264.
King, G.M., and Weber, C.F. (2007) Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat Rev Microbiol 5: 107-118.
Knief, C., Delmotte, N., Chaffron, S., Stark, M., Innerebner, G., Wassmann, R., et al. (2012) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6: 1378-1390.
Knief, C., Ramette, A., Frances, L., Alonso-Blanco, C., and Vorholt, J.A. (2010) Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J 4: 719-728.
Kumar, S., Stecher, G., and Tamura, K. (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33: 1870-1874.
Lalonde, I., and Constant, P. (2016) Identification of unknown carboxydovore bacteria dominant in deciduous forest soil via succession of bacterial communities, coxL genotypes, and carbon monoxide oxidation activity in soil microcosms. Appl Environ Microbiol 82: 1324-1333.
Lelieveld, J., Evans, J.S., Fnais, M., Giannadaki, D., and Pozzer, A. (2015) The contribution of outdoor air pollution sources to premature mortality on a global scale. Nature 525: 367-371.
Leveau, J.H., and Lindow, S.E. (2001) Appetite of an epiphyte: quantitative monitoring of bacterial sugar consumption in the phyllosphere. Proc Natl Acad Sci 98: 3446-3453.
Lindow, S.E., and Brandl, M.T. (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69: 1875-1883.
Liu, H., Tian, Y., Xiang, X., Li, M., Wu, Y., Cao, Y., et al. (2018) Association of short-term exposure to ambient carbon monoxide with hospital admissions in China. Sci Rep 8: 1-7.
Lorite, M.J., Tachil, J., Sanjuan, J., Meyer, O., and Bedmar, E.J. (2000) Carbon monoxide dehydrogenase activity in Bradyrhizobium japonicum. Appl Environ Microbiol 66: 1871-1876.
Love, M.I., Huber, W., and Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15: 550.
Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, B., et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
Lyons, C.M., Justin, P., Colby, J., and Williams, E. (1984) Isolation, characterization and autotrophic metabolism of a moderately thermophilic carboxydobacterium, Pseudomonas thermocarboxydovorans sp-nov. J Gen Microbiol 130: 1097-1105.
McDonald, D., Price, M.N., Goodrich, J., Nawrocki, E.P., DeSantis, T.Z., Probst, A., et al. (2012) An improved greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6: 610-618.
Mercier, J., and Lindow, S. (2000) Role of leaf surface sugars in colonization of plants by bacterial epiphytes. Appl Environ Microbiol 66: 369-374.
Meyer, O., and Schlegel, H.G. (1983) Biology of aerobic carbon-monoxide oxidizing bacteria. Annu Rev Microbiol 37: 277-310.
Moran, M.A., Buchan, A., Gonzalez, J.M., Heidelberg, J.F., Whitman, W.B., Kiene, R.P., et al. (2004) Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432: 910-913.
Nadalig, T., Farhan Ul Haque, M., Roselli, S., Schaller, H., Bringel, F., and Vuilleumier, S. (2011) Detection and isolation of chloromethane-degrading bacteria from the Arabidopsis thaliana phyllosphere, and characterization of chloromethane utilization genes. FEMS Microbiol Ecol 77: 438-448.
Novelli, P., Masarie, K., and Lang, P. (1998) Distributions and recent changes of carbon monoxide in the lower troposphere. J Geophys Res Atmos 103: 19015-19033.
Ou-Yang, C.-F., Lin, N.-H., Lin, C.-C., Wang, S.-H., Sheu, G.-R., Lee, C.-T., et al. (2014) Characteristics of atmospheric carbon monoxide at a high-mountain background station in East Asia. Atmos Environ 89: 613-622.
Park, S.W., Hwang, E.H., Park, H., Kim, J.A., Heo, J., Lee, K.H., et al. (2003) Growth of mycobacteria on carbon monoxide and methanol. J Bacteriol 185: 142-147.
Parte, A.C., Sardà Carbasse, J., Meier-Kolthoff, J.P., Reimer, L.C., and Göker, M. (2020) List of prokaryotic names with standing in nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 70: 5607-5612.
Redford, A.J., Bowers, R.M., Knight, R., Linhart, Y., and Fierer, N. (2010) The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ Microbiol 12: 2885-2893.
Reeves, C.E., Penkett, S.A., Bauguitte, S., Law, K.S., Evans, M.J., Bandy, B.J., et al. (2002) Potential for photochemical ozone formation in the troposphere over the North Atlantic as derived from aircraft observations during ACSOE. J Geophys Res-Atmos 107: 1-14.
Remus-Emsermann, M.N., Tecon, R., Kowalchuk, G.A., and Leveau, J.H. (2012) Variation in local carrying capacity and the individual fate of bacterial colonizers in the phyllosphere. ISME J 6: 756-765.
Saitou, N., and Nei, M. (1987) The neighbor-joining method - a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
Sandhu, A., Halverson, L.J., and Beattie, G.A. (2009) Identification and genetic characterization of phenol-degrading bacteria from leaf microbial communities. Microb Ecol 57: 276-285.
Scheublin, T.R., and Leveau, J.H.J. (2013) Isolation of Arthrobacter species from the phyllosphere and demonstration of their epiphytic fitness. Microbiology 2: 205-213.
Seiler, W., and Giehl, H. (1977) Influence of plants on atmospheric carbon-monoxide. Geophys Res Lett 4: 329-332.
Stubbins, A., Uher, G., Law, C.S., Mopper, K., Robinson, C., and Upstill-Goddard, R.C. (2006) Open-ocean carbon monoxide photoproduction. Deep-Sea Res II Top Stud Oceanogr 53: 1695-1705.
Tarr, M.A., Miller, W.L., and Zepp, R.G. (1995) Direct carbon-monoxide photoproduction from plant matter. J Geophys Res-Atmos 100: 11403-11413.
Tolli, J.D., Sievert, S.M., and Taylor, C.D. (2006) Unexpected diversity of bacteria capable of carbon monoxide oxidation in a coastal marine environment, and contribution of the Roseobacter-associated clade to total CO oxidation. Appl Environ Microbiol 72: 1966-1973.
Tolli, J.D., and Taylor, C.D. (2005) Biological CO oxidation in the Sargasso Sea and in vineyard sound, Massachusetts. Limnol Oceanogr 50: 1205-1212.
Venter, J.C., Remington, K., Heidelberg, J.F., Halpern, A.L., Rusch, D., Eisen, J.A., et al. (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66-74.
Vogel, C., Innerebner, G., Zingg, J., Guder, J., and Vorholt, J.A. (2012) Forward genetic in planta screen for identification of plant-protective traits of Sphingomonas sp. strain Fr1 against pseudomonas syringae DC3000. Appl Environ Microbiol 78: 5529-5535.
Vorholt, J.A. (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10: 828-840.
Wang, Q., Garrity, G.M., Tiedje, J.M., and Cole, J.R. (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.
Weber, C.F., and King, G.M. (2010) Distribution and diversity of carbon monoxide-oxidizing bacteria and bulk bacterial communities across a succession gradient on a Hawaiian volcanic deposit. Environ Microbiol 12: 1855-1867.
Weber, C.F., and King, G.M. (2017) Volcanic soils as sources of novel CO-oxidizing Paraburkholderia and Burkholderia: Paraburkholderia hiiakae sp nov., Paraburkholderia metrosideri sp nov., Paraburkholderia paradisi sp nov., Paraburkholderia peleae sp nov., and Burkholderia alpina sp nov a member of the Burkholderia cepacia complex. Front Microbiol 8(207): 1-10.
Weisburg, W.G., Barns, S.M., Pelletier, D.A., and Lane, D.J. (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173: 697-703.
Westberg, K., Cohen, N., and Wilson, K.W. (1971) Carbon monoxide - its role in photochemical smog formation. Science 171: 1013-1015.
Whipps, J.M., Hand, P., Pink, D., and Bending, G.D. (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105: 1744-1755.
Woodward, F., and Lomas, M. (2004) Vegetation dynamics-simulating responses to climatic change. Biol Rev 79: 643-670.
Wu, X.H., Ge, T.D., Hu, Y.J., Wei, X.M., Chen, L., Whiteley, A.S., and Wu, J.S. (2017) Abundance and diversity of carbon monoxide dehydrogenase genes from BMS clade bacteria in different vegetated soils. Eur J Soil Biol 81: 94-99.
Xie, H.X., Zafiriou, O.C., Umile, T.P., and Kieber, D.J. (2005) Biological consumption of carbon monoxide in Delaware Bay, NW Atlantic and Beaufort Sea. Mar Ecol Prog Ser 290: 1-14.
Xu, L., Zhang, Y., Mohamad, O.A., Jiang, C., and Friman, V.-P. (2018) Mesorhizobium zhangyense sp. nov., isolated from wild Thermopsis lanceolate in northwestern China. Arch Microbiol 200: 603-610.
Xue, M., Wang, Y.S., Sun, Y., Hu, B., and Wang, M.X. (2006) Measurement on the atmospheric CO concentration in Beijing. Environ Sci 27: 200-206.
Yang, J., Zhou, E.M., Jiang, H.C., Li, W.J., Wu, G., Huang, L.Q., et al. (2015) Distribution and diversity of aerobic carbon monoxide-oxidizing bacteria in geothermal springs of China, The Philippines, and the United States. Geomicrobiol J 32: 903-913.
Yutthammo, C., Thongthammachat, N., Pinphanichakarn, P., and Luepromchai, E. (2010) Diversity and activity of PAH-degrading bacteria in the phyllosphere of ornamental plants. Microb Ecol 59: 357-368.