Summary:
The global emission of methane (CH4) is estimated to be 500-600 Tg per year from diverse natural and man-made sources. Wetlands are the main source of methane and provide an ideal habitat for anaerobic methanogenic archaea which significantly contribute to the total global methane emission. Besides permanently flooded wetlands, there are distinct wetlands created by small water bodies within parts of plants, called phytotelmata. These water catchments in tropical forests comprise bamboo nodes, pitcher plants, tree holes, tank bromeliads and non-bromeliads leaf axils. Recent work indicates that phytotelmata may contribute to the global methane budget. Tank bromeliads, which effectively collect rainwater and organic substrate between their leaf axils (tank slurry), emit substantial amounts of methane into the atmosphere over neotropical forests. However, studies on the microbial communities involved in methane cycling and environmental factors which influence their activity are still rare. In the present study we established tank bromeliads as a model system in the greenhouse and collected field data to investigate the microbial communities in tank bromeliads.
Investigation of Costa Rican tank bromeliads revealed that inhabiting microbial communities (Bacteria, Archaea) differed between individual plants, although the plants belong to the same species and were growing in the same habitat patch. Major determinants for the individual plants microbial community composition were carbon, nitrogen, oxygen concentrations, and the pH of tank slurries. These factors depend on the incoming rainwater, leaf litter or input by higher organisms (e.g. insects, spiders, birds). Therefore, the site where a tank bromeliad develops may play an important role for the inhabiting microbial communities. In summary, our results indicate that every bromeliad tank is a unique island with respect to its resident microbial community. The presence of methanogens and methanotrophs in all tank slurries further indicates the potential for both methane formation and methane oxidation in the bromeliad tanks.
Besides tank slurry properties we have shown that the availability of water shapes the archaeal and bacterial community in tank bromeliads. Increasing drought resulted in a decrease of methane formation and in a shift from a hydrogenotrophic dominated community (Methanobacteriales) to an aceticlastic (Methanosaetaceae) dominated methanogenic community. This trend was also observed in the isotopic signature of produced methane and so hydrogenotrophically derived methane dominated under high moisture. Increasing drought resulted in increasing oxygen exposure for the microoorganisms. We found genes for oxygen detoxifying enzymes in genomes of Methanosaeta species, indicating that these methanogens are more oxygen tolerant than previously assumed. With increasing drought the relative abundance of the Burkholderiales, mainly represented by the genus Burkholderia, more than tripled in tank slurry whereas the bacterial diversity decreased. Furthermore, regardless of the water content or the incubation environment (inside or outside of bromeliad tanks) the genus Burkholderia was the most abundant group, indicating its tolerance towards changing water levels which frequently occur in tank bromeliads under natural conditions. Upon drought gene copy numbers of nifH, a marker gene for nitrogen fixation known to occur in Burkolderia spp. as well as Methanosaeta spp., increased. Therefore, this work indicates that tank bromeliads inhabiting microbes are not only involved in carbon cycling but also in nitrogen cycling.
We further investigated the potential of methane formation in non-bromeliad leaf axils. The leaf axils of oil palms create catchments similar to the leaf axils of tank bromeliads where organic matter and rainwater accumulate. In incubation experiments we showed that under water-logged oxic or anoxic conditions methane is formed in this organic material, accompanied by increasing gene copy numbers of mcrA, a commonly used marker gene for methanogens. Therefore, our results indicate that leaf axils of oil palms seem to be a potential habitat for methanogenesis.
The results of this work give new insights into the microbial communities and methane cycling in plant leaf axils and emphasize the need to better resolve the role of phytotelmata in the cycling of methane to better understand the global methane budget.
Bibliographie / References
- Yavitt JB (2010) Biogeochemistry: Cryptic wetlands. Nat Geosci 3:749-750
- Großkopf R, Janssen PH, Liesack W (1998) Diversity and structure of the methanogenic community in anoxic rice paddy soil microcosms as examined by cultivation and direct 16S rRNA gene sequence retrieval. Appl Environ Microbiol 64:960-969
- Zehnder AJB, Stumm W (1988) Geochemistry and biogeochemistry of anaerobic habitats.
- Patrick WH Jr, Reddy CN (1978) " Chemical changes in rice soils " , in: International Rice Research Institute (ed.), Soils and rice, IRRI, Los Banos, Philippines, 361-379
- Zotz G, Thomas V (1999) How much water is in the tank? Model calculations for two epiphytic bromeliads. Ann Bot 83:183-192
- Ponnamperuma FN (1972) The chemistry of submerged soils. Adv Agron 24:29-96
- Malhi Y, Roberts JT, Betts RA, Killeen TJ, Li W, Nobre CA (2008) Climate change, deforestation, and the fate of the Amazon. Science 319:169-172
- Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, et al. (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046-2056
- Hofhansl F, Kobler J, Ofner J, Drage S, Pölz E-M, Wanek W (2014) Sensitivity of tropical forest aboveground productivity to climate anomalies in SW Costa Rica. Global Biogeochem Cy 28, doi:10.1002/2014GB004934.
- Salazar LF, Nobre CA, Oyama MD (2007) Climate change consequences on the biome distribution in tropical South America. Geophys Res Lett 34, L09708 doi:10.1029/2007GL029695.
- Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PloS one 6:e27310
- Bolker JA (1994) Model systems in developmental biology. BioEssays 17:451-455
- Goffredi SK, Kantor AH, Woodside WT (2011b) Aquatic microbial habitats within a neotropical rainforest: bromeliads and pH-associated trends in bacterial diversity and composition. Microb Ecol 61:529-542
- Srivastava DS (2006) Habitat structure, trophic structure and ecosystem function: interactive effects in a bromeliad–insect community. Oecologia 149:493-504
- Wei J, Liu X, Wang Q, Wang C, Chen X, Li H (2014) Effect of rhizodeposition on pyrene bioaccessibility and microbial structure in pyrene and pyrene–lead polluted soil. Chemosphere 97:92-97
- Osborne CA, Galic M, Sangwan P, Janssen PH (2005) PCR‐generated artefact from 16S rRNA gene‐specific primers. FEMS Microbiol Lett 248:183-187
- Watanabe T, Kimura M, Asakawa S (2009) Distinct members of a stable methanogenic archaeal community transcribe mcrA genes under flooded and drained conditions in Japanese paddy field soil. Soil Biol Biochem 41:276-285
- Martinson GO, Werner FA, Scherber C, Conrad R, Corre MD, Flessa H, Wolf K, Klose M, Gradstein SR, Veldkamp E (2010) Methane emissions from tank bromeliads in neotropical forests. Nat Geosci 3:766-769
- Pankratov TA, Tindall BJ, Liesack W, Dedysh SN (2007) Mucilaginibacter paludis gen. nov., sp. nov. and Mucilaginibacter gracilis sp. nov., pectin-, xylan-and laminarin-degrading members of the family Sphingobacteriaceae from acidic Sphagnum peat bog. Int J Syst Evol Microbiol 57:2349-2354
- Richardson BA (1999) The Bromeliad microcosm and the assessment of faunal diversity in a Neotropical forest. Biotropica 31:321-336
- Krieger JR, Kourtev PS (2012) Detection of methanogenic archaea in the pitchers of the Northern pitcher plant (Sarracenia purpurea). Can J Microbiol 58:189-194
- Brouard O, Le Jeune AH, Leroy C, Cereghino R, Roux O, Pelozuelo L, Dejean A, Corbara B, Carrias JF (2011) Are algae relevant to the detritus-based food web in tank-bromeliads?. PloS One 6:e20129
- Angel R, Matthies D, Conrad R (2011) Activation of methanogenesis in arid biological soil crusts despite the presence of oxygen. PLoS One 6:20453
- Noll M, Klose M, Conrad R (2010) Effect of temperature change on the composition of the bacterial and archaeal community potentially involved in the turnover of acetate and propionate in methanogenic rice field soil. FEMS Microbiol Ecol 73:215-225
- Brandt FB, Martinson GO, Pommerenke B, Pump J, Conrad R (2014) Drying effects on archaeal community composition and methanogenesis in bromeliad tanks. FEMS Microbiol Ecol, doi.org/10.1093/femsec/fiu021.
- Keith KE, Valvano MA (2007) Characterization of SodC, a periplasmic superoxide dismutase from Burkholderia cenocepacia. Infect Immun 75:2451-2460
- Springer E, Sachs MS, Woese CR, Boone DR (1995) Partial gene sequences for the A subunit of methyl-coenzyme M reductase (mcrI) as a phylogenetic tool for the family Methanosarcinaceae. Int J of Sys Bacteriol 45:554-559
- Pankratov TA, Kirsanova LA, Kaparullina EN, Kevbrin VV, Dedysh SN (2012) Telmatobacter bradus gen. nov., sp. nov., a cellulolytic facultative anaerobe from subdivision 1 of the Acidobacteria, and emended description of Acidobacterium capsulatum Kishimoto, et al.
- Barber RD, Zhang L, Harnack M, Olson MV, Kaul R, Ingram-Smith C, Smith KS (2011) Complete genome sequence of Methanosaeta concilii, a specialist in aceticlastic methanogenesis. J Bacteriol 193:3668-3669
- Carrias JF, Cussac ME, Corbara B (2001) A preliminary study of freshwater protozoa in tank bromeliads. J Trop Ecol 17:611-617
- Stuntz S, Ziegler C, Simon U, Zotz G (2002) Diversity and structure of the arthropod fauna within three canopy epiphyte species in central Panama. J Trop Ecol 18:161-176
- Zehnder AJB (ed.), Biology of Anaerobic Microorganisms, Wiley-Interscience, New York, pp 1–38 Discussion and concluding remarks
- Weimer PJ, Zeikus JG (1978) Acetate metabolism in Methanosarcina barkeri. Arch Microbiol 119:175-182
- Rovira AD (1969) Plant root exudates. Bot Rev 35:35-57
- Carmichael MJ, Bernhardt ES, Bräuer SL, Smith WK (2014) The role of vegetation in methane flux to the atmosphere: should vegetation be included as a distinct category in the global methane budget?. Biogeochemistry 119:1-24
- Lopez LCS, Alves RRDN, Rios RI (2009) Micro-environmental factors and the endemism of bromeliad aquatic fauna. Hydrobiologia 625:151-156
- Pittl E, Innerebner G, Wanek W, Insam H (2010) Microbial communities of arboreal and ground soils in the Esquinas rainforest, Costa Rica. Plant Soil 329:65-74
- Stewart GR, Schmidt S, Handley LL, Turnbull MH, Erskine PD, Joly CA (1995) 15 N natural abundance of vascular rainforest epiphytes: implications for nitrogen source and acquisition. Plant Cell Environ 18:85-90
- Drying effects on bacterial community
- Kitching RL (2001) Food webs in phytotelmata: " bottom-up " and " top-down " explanations for community structure. Annu Rev Entomol 46:729-760
- Verheye W (2010) Growth and production of oil palm. Land use, land cover and soil sciences. Encyclopedia of Life Support Systems (EOLSS). UNESCO-EOLSS Publishers, Oxford, UK
- Suleiman M, Brandt FB, Brenzinger K, Martinson GO (in preparation). Leaf axils of oil palms-a potential habitat for denitrification
- Muyzer G, Teske A, Wirsen CO, Jannasch HW (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164:165- 172
- Ridley HN (1930) Plants can grow as epiphytes in the leaf axils of oil palm trees The Dispersal of Plants Throughout the World. L. Reeve & Co., Kent, UK Schlesinger WH, Bernhardt ES (1997) Biogeochemistry: An Analysis of Global Change, 2nd ed, Academic Press, San Diego, CA
- Suárez-Moreno ZR, Caballero-Mellado J, Venturi V (2008) The new group of non- pathogenic plant-associated nitrogen-fixing Burkholderia spp. shares a conserved quorum-sensing system, which is tightly regulated by the RsaL repressor. Microbiology 154:2048-2059
- Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web- based tools. Nucleic Acids Res gks1219
- Cox PM, Harris PP, Huntingford C, Betts RA, Collins M, Jones CD, Jupp TE, Marengo JA, Nobre CA (2008) Increasing risk of Amazonian drought due to decreasing aerosol pollution. Nature 453:212-215 Discussion and concluding remarks
- Kotowska MM, Werner FA (2013) Environmental controls over methane emissions from bromeliad phytotelmata: The role of phosphorus and nitrogen availability, temperature, and water content. Global Biogeoch Cy 27:1186-1193
- Wu XL, Conrad R (2001) Functional and structural response of a cellulose‐degrading methanogenic microbial community to multiple aeration stress at two different temperatures. Environ Microbiol 3:355-362
- Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173:600-610
- Inselsbacher E, Cambui CA, Richter A, Stange CF, Mercier H, Wanek W (2007) Microbial activities and foliar uptake of nitrogen in the epiphytic bromeliad Vriesea gigantea. New Phytol 175:311-320
- Marino NA, Srivastava DS, Farjalla VF (2013) Aquatic macroinvertebrate community composition in tank‐bromeliads is determined by bromeliad species and its constrained characteristics. Insect Conserv Divers 6:372-380
- Koh LP, Wilcove DS (2008) Is oil palm agriculture really destroying tropical biodiversity?. Conserv Lett 1:60-64
- Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann NY Acad Sci 1125:171-189
- Cabiscol E, Tamarit J, Ros J (2010) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3:3-8
- Hu BL, Shen LD, Lian X, Zhu Q, Liu S, Huang Q, et al. (2014) Evidence for nitrite-dependent anaerobic methane oxidation as a previously overlooked microbial methane sink in wetlands. PNAS 111:4495-4500
- Peters V, Conrad R (1995) Methanogenic and other strictly anaerobic bacteria in desert soil and other oxic soils. Appl Environ Microbiol 61:1673–1676
- Janssen PH, Frenzel P (1997) Inhibition of methanogenesis by methyl fluoride: studies of pure and defined mixed cultures of anaerobic bacteria and archaea. Appl Environ Microbiol 63:4552-4557
- Caballero-Mellado J, Onofre-Lemus J, Estrada-de los Santos P, Martínez-Aguilar L (2007) The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Micobiol 73:5308- 5319
- Goffredi SK, Jang GE, Woodside WT, Ussler W (2011a) Bromeliad catchments as habitats for methanogenesis in tropical rainforest canopies. Front Microbiol 2:529-542
- Poly F, Ranjard L, Nazaret S, Gourbière F, Monrozier LJ (2001) Comparison of nifH gene pools in soils and soil microenvironments with contrasting properties. Appl Environ Microbiol 67:2255-2262
- Deutzmann JS, Stief P, Brandes J, Schink B (2014) Anaerobic methane oxidation coupled to denitrification is the dominant methane sink in a deep lake. PNAS 111:18273-18278
- Carmo FL, Santos HF, Peixoto RS, Rosado AS, Araujo FV (2014) Tank bromeliad water: similar or distinct environments for research of bacterial bioactives? Braz J Microbiol 45:185-192
- Cai Z, Yan X (1999) Kinetic model for methane oxidation by paddy soil as affected by temperature, moisture and N addition. Soil Biol Biochem 31:715-725
- Stubner S (2002) Enumeration of 16S rDNA of Desulfotomaculum lineage 1 in rice field soil by real-time PCR with SybrGreen™ detection. J Microbiol Methods 50:155-164
- Jessup CM, Kassen R, Forde SE, KerrB, Buckling A, Rainey PB, Bohannan BJ (2004) Big questions, small worlds: microbial model systems in ecology. Trends Ecol Evol 19:189-197
- Srivastava DS, Kolasa J, Bengtsson J, Gonzalez A, Lawler SP, Miller TE, et al. (2004) Are natural microcosms useful model systems for ecology?. Trends Ecol Evol 19: 379-384
- Reijnders L, Huijbregts MAJ (2008) Palm oil and the emission of carbon-based greenhouse gases. J Clean Prod 16:477-482
- Le Mer J, Roger P (2001) Production, oxidation, emission and consumption of methane by soils: a review. Eur J Soil Biol 37:25-50