Elevated methane flux in a tropical peatland post-fire is linked to depth-dependent changes in peat microbiome assembly.
Journal
NPJ biofilms and microbiomes
ISSN: 2055-5008
Titre abrégé: NPJ Biofilms Microbiomes
Pays: United States
ID NLM: 101666944
Informations de publication
Date de publication:
23 Jan 2024
23 Jan 2024
Historique:
received:
27
04
2023
accepted:
08
01
2024
medline:
23
1
2024
pubmed:
23
1
2024
entrez:
22
1
2024
Statut:
epublish
Résumé
Fires in tropical peatlands extend to depth, transforming them from carbon sinks into methane sources and severely limit forest recovery. Peat microbiomes influence carbon transformations and forest recovery, yet our understanding of microbiome shifts post-fire is currently limited. Our previous study highlighted altered relationships between the peat surface, water table, aboveground vegetation, and methane flux after fire in a tropical peatland. Here, we link these changes to post-fire shifts in peat microbiome composition and assembly processes across depth. We report kingdom-specific and depth-dependent shifts in alpha diversity post-fire, with large differences at deeper depths. Conversely, we found shifts in microbiome composition across all depths. Compositional shifts extended to functional groups involved in methane turnover, with methanogens enriched and methanotrophs depleted at mid and deeper depths. Finally, we show that community shifts at deeper depths result from homogeneous selection associated with post-fire changes in hydrology and aboveground vegetation. Collectively, our findings provide a biological basis for previously reported methane fluxes after fire and offer new insights into depth-dependent shifts in microbiome assembly processes, which ultimately underlie ecosystem function predictability and ecosystem recovery.
Identifiants
pubmed: 38253600
doi: 10.1038/s41522-024-00478-9
pii: 10.1038/s41522-024-00478-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8Subventions
Organisme : Ministry of Education - Singapore (MOE)
ID : FY2015-SUG
Informations de copyright
© 2024. The Author(s).
Références
Dargie, G. C. et al. Age, extent and carbon storage of the central Congo Basin peatland complex. Nature 542, 86–90 (2017).
pubmed: 28077869
Page, S. E., Rieley, J. O. & Banks, C. J. Global and regional importance of the tropical peatland carbon pool. Glob. Change Biol. 17, 798–818 (2011).
Page, S. E. & Hooijer, A. In the line of fire: the peatlands of Southeast Asia. Philos. Trans. R. Soc. B: Biol. Sci. 371, 20150176 (2016).
Turetsky, M. R. et al. Global vulnerability of peatlands to fire and carbon loss. Nat. Geosci. 8, 11–14 (2015).
Page, S. et al. Anthropogenic impacts on lowland tropical peatland biogeochemistry. Nat. Rev. Earth Environ. 2022 3:7 3, 426–443 (2022).
Smith, S. M., Newman, S., Garrett, P. B. & Leeds, J. A. Differential effects of surface and peat fire on soil constituents in a degraded wetland of the Northern Florida Everglades. J. Environ. Qual. 30, 1998–2005 (2001).
pubmed: 11790006
Rein, G., Cleaver, N., Ashton, C., Pironi, P. & Torero, J. L. The severity of smouldering peat fires and damage to the forest soil. CATENA 74, 304–309 (2008).
Könönen, M., Jauhiainen, J., Laiho, R., Kusin, K. & Vasander, H. Physical and chemical properties of tropical peat under stabilised land uses. Mires peat 16, 1–13 (2015).
Lupascu, M., Akhtar, H., Smith, T. E. L. & Sukri, R. S. Post-fire carbon dynamics in the tropical peat swamp forests of Brunei reveal long-term elevated CH4 flux. Glob. Change Biol. 26, 5125–5145 (2020).
Wösten, J. H. M. et al. Interrelationships between hydrology and ecology in fire degraded tropical peat swamp forests. Int. J. Water Resour. Dev. 22, 157–174 (2006).
Page, S. et al. Restoration ecology of lowland tropical peatlands in Southeast Asia: Current knowledge and future research directions. Ecosystems 12, 888–905 (2009).
Sáenz de Miera, L. E., Pinto, R., Gutierrez-Gonzalez, J. J., Calvo, L. & Ansola, G. Wildfire effects on diversity and composition in soil bacterial communities. Sci. Total Environ. 726, 138636 (2020).
pubmed: 32320886
Nelson, A. R. et al. Wildfire-dependent changes in soil microbiome diversity and function. Nat. Microbiol. 7, 1419–1430 (2022).
pubmed: 36008619
pmcid: 9418001
Pressler, Y., Moore, J. C. & Cotrufo, M. F. Belowground community responses to fire: meta-analysis reveals contrasting responses of soil microorganisms and mesofauna. Oikos 128, 309–327 (2019).
Brown, S. P. et al. Context dependent fungal and bacterial soil community shifts in response to recent wildfires in the Southern Appalachian Mountains. For. Ecol. Manag. 451, 117520 (2019).
Whitman, T. et al. Soil bacterial and fungal response to wildfires in the Canadian boreal forest across a burn severity gradient. Soil Biol. Biochem. 138, 107571 (2019).
Taş, N. et al. Impact of fire on active layer and permafrost microbial communities and metagenomes in an upland Alaskan boreal forest. ISME J. 8, 1904–1919 (2014).
pubmed: 24722629
pmcid: 4139727
Yang, S. et al. Fire affects the taxonomic and functional composition of soil microbial communities, with cascading effects on grassland ecosystem functioning. Glob. Change Biol. 26, 431–442 (2020).
Dove, N. C., Taş, N. & Hart, S. C. Ecological and genomic responses of soil microbiomes to high-severity wildfire: linking community assembly to functional potential. ISME J. 16, 1853–1863 (2022).
pubmed: 35430593
pmcid: 9213548
Sazawa, K. et al. Impact of peat fire on the soil and export of dissolved organic carbon in tropical peat soil, Central Kalimantan, Indonesia. ACS Earth Space Chem. 2, 692–701 (2018).
Averill, C., Werbin, Z. R., Atherton, K. F., Bhatnagar, J. M. & Dietze, M. C. Soil microbiome predictability increases with spatial and taxonomic scale. Nat. Ecol. Evolution 5, 747–756 (2021).
Ferrenberg, S. et al. Changes in assembly processes in soil bacterial communities following a wildfire disturbance. ISME J. 7, 1102–1111 (2013).
pubmed: 23407312
pmcid: 3660671
Xiang, X. et al. Rapid recovery of soil bacterial communities after wildfire in a Chinese boreal forest. Sci. Rep. 4, 3829 (2014).
pubmed: 24452061
pmcid: 3899593
Lee, S.-H., Sorensen, J. W., Grady, K. L., Tobin, T. C. & Shade, A. Divergent extremes but convergent recovery of bacterial and archaeal soil communities to an ongoing subterranean coal mine fire. ISME J. 11, 1447–1459 (2017).
pubmed: 28282042
pmcid: 5437352
Turner, M. G., Smithwick, E. A. H., Metzger, K. L., Tinker, D. B. & Romme, W. H. Inorganic nitrogen availability after severe stand-replacing fire in the Greater Yellowstone ecosystem. Proc. Natl. Acad. Sci. 104, 4782–4789 (2007).
pubmed: 17360349
pmcid: 1829215
Ning, D. et al. A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming. Nat. Commun. 11, 4717 (2020).
pubmed: 32948774
pmcid: 7501310
Fodelianakis, S. et al. Microdiversity characterizes prevalent phylogenetic clades in the glacier-fed stream microbiome. ISME J. 16, 666–675 (2022).
pubmed: 34522009
Akhtar, H., Lupascu, M. & Sukri, R. S. Interactions between microtopography, root exudate analogues and temperature determine CO2 and CH4 production rates in fire-degraded tropical peat. Soil Biol. Biochem. 169, 108646 (2022).
Akhtar, H. et al. Significant sedge-mediated methane emissions from degraded tropical peatlands. Environ. Res. Lett. 16, 014002 (2021).
Girkin, N. T., Vane, C. H., Turner, B. L., Ostle, N. J. & Sjögersten, S. Root oxygen mitigates methane fluxes in tropical peatlands. Environ. Res. Lett. 15, 064013 (2020).
Certini, G. Effects of fire on properties of forest soils: a review. Oecologia 143, 1–10 (2005).
pubmed: 15688212
Stegen, J. C. At the nexus of history, ecology, and hydrobiogeochemistry: Improved predictions across scales through integration. mSystems 3, e00167–17 (2018).
pubmed: 29657967
pmcid: 5895879
Vellend, M. Conceptual synthesis in community ecology. Q. Rev. Biol. 85, 183–206 (2010).
pubmed: 20565040
Nemergut, Diana et al. Patterns and processes of microbial community assembly. Microbiol. Mol. Biol. Rev. 77, 342–356 (2013).
pubmed: 24006468
pmcid: 3811611
Evans, S., Martiny, J. B. H. & Allison, S. D. Effects of dispersal and selection on stochastic assembly in microbial communities. ISME J. 11, 176–185 (2017).
pubmed: 27494293
West, J. R. & Whitman, T. Disturbance by soil mixing decreases microbial richness and supports homogenizing community assembly processes. FEMS Microbiol. Ecol. 98, fiac089 (2022).
pubmed: 35869965
pmcid: 9397575
Andersen, R., Chapman, S. J. & Artz, R. R. E. Microbial communities in natural and disturbed peatlands: A review. Soil Biol. Biochem. 57, 979–994 (2013).
Allingham, S. M., Nwaishi, F. C., Andersen, R., Lamit, L. J. & Elliott, D. R. Microbial communities and biogeochemical functioning across peatlands in the Athabasca Oil Sands region of Canada: Implications for reclamation and management. Land Degrad. Dev. 34, 1504–1521 (2023).
Seward, J. et al. Peatland Microbial Community Composition Is Driven by a Natural Climate Gradient. Microb. Ecol. 80, 593–602 (2020).
pubmed: 32388577
Zhu, A., Ibrahim, J. G. & Love, M. I. Heavy-tailed prior distributions for sequence count data: removing the noise and preserving large differences. Bioinformatics 35, 2084–2092 (2019).
pubmed: 30395178
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 1–21 (2014).
Nottingham, A. T. et al. Microbial diversity declines in warmed tropical soil and respiration rise exceed predictions as communities adapt. Nat. Microbiol. 7, 1650–1660 (2022).
pubmed: 36065063
Belmok, A. et al. Long-term effects of periodical fires on archaeal communities from Brazilian Cerrado Soils. Archaea 2019, 6957210 (2019).
pubmed: 30833827
pmcid: 6369511
Pérez-Valera, E., Verdú, M., Navarro-Cano, J. A. & Goberna, M. Resilience to fire of phylogenetic diversity across biological domains. Mol. Ecol. 27, 2896–2908 (2018).
pubmed: 29802784
Valentine, D. L. Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat. Rev. Microbiol. 5, 316–323 (2007).
pubmed: 17334387
Kassen, R. The experimental evolution of specialists, generalists, and the maintenance of diversity. J. Evolut. Biol. 15, 173–190 (2002).
Zhou, Z., Pan, J., Wang, F., Gu, J.-D. & Li, M. Bathyarchaeota: globally distributed metabolic generalists in anoxic environments. FEMS Microbiol. Rev. 42, 639–655 (2018).
pubmed: 29790926
Tripathi, B. M. et al. pH dominates variation in tropical soil archaeal diversity and community structure. FEMS Microbiol. Ecol. 86, 303–311 (2013).
pubmed: 23773164
Adam, P. S., Borrel, G., Brochier-Armanet, C. & Gribaldo, S. The growing tree of Archaea: new perspectives on their diversity, evolution and ecology. The. ISME J. 11, 2407–2425 (2017).
pubmed: 28777382
pmcid: 5649171
Sun, H. et al. Bacterial community structure and function shift across a northern boreal forest fire chronosequence. Sci. Rep. 6, 32411 (2016).
pubmed: 27573440
pmcid: 5004109
Serrano-Silva, N., Sarria-GuzmÁN, Y., Dendooven, L. & Luna-Guido, M. Methanogenesis and methanotrophy in Soil: A review. Pedosphere 24, 291–307 (2014).
Gandois, L. et al. Origin, composition, and transformation of dissolved organic matter in tropical peatlands. Geochimica et. Cosmochimica Acta 137, 35–47 (2014).
Wilson, R. M. et al. Stability of peatland carbon to rising temperatures. Nat. Commun. 7, 13723 (2016).
pubmed: 27958276
pmcid: 5159855
Tfaily, M. M. et al. Organic matter transformation in the peat column at Marcell Experimental Forest: Humification and vertical stratification. J. Geophys. Res.: Biogeosciences 119, 661–675 (2014).
Chanton, J. P. et al. Radiocarbon evidence for the importance of surface vegetation on fermentation and methanogenesis in contrasting types of boreal peatlands. Global Biogeochem. Cycles 22, 1–11 (2008).
Oremland Ronald, S. & Polcin, S. Methanogenesis and sulfate reduction: Competitive and noncompetitive substrates in estuarine sediments. Appl. Environ. Microbiol. 44, 1270–1276 (1982).
pmcid: 242184
Oremland, R. S., Marsh, L. M. & Polcin, S. Methane production and simultaneous sulphate reduction in anoxic, salt marsh sediments. Nature 296, 143–145 (1982).
Garcia, P. S., Gribaldo, S. & Borrel, G. Diversity and evolution of methane-related pathways in Archaea. Annu. Rev. Microbiol. 76, 727–755 (2022).
pubmed: 35759872
Evans, P. N. et al. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350, 434–438 (2015).
pubmed: 26494757
Gil Joshua, C. & Hird Sarah, M. Multiomics characterization of the canada goose fecal microbiome reveals selective efficacy of simulated metagenomes. Microbiol. Spectr. 10, e02384–02322 (2022).
pubmed: 36318011
pmcid: 9769641
Bräuer, S. L., Basiliko, N., Siljanen, H. M. P. & Zinder, S. H. Methanogenic archaea in peatlands. FEMS Microbiol. Lett. 367, fnaa172, (2020).
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10–12 (2011).
Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).
pubmed: 27214047
pmcid: 4927377
Quast, C. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, 590–596 (2013).
Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments. PLOS ONE 5, e9490 (2010).
pubmed: 20224823
pmcid: 2835736
Wright, E. S. RNAconTest: comparing tools for noncoding RNA multiple sequence alignment based on structural consistency. RNA 26, 531–540 (2020).
pubmed: 32005745
pmcid: 7161358
R: A language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, Austria., 2023).
McMurdie, P. J. & Holmes, S. phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLOS ONE 8, e61217 (2013).
pubmed: 23630581
pmcid: 3632530
Oksanen, J. et al. Package ‘vegan’. Community Ecol. package, version 2, 1–295 (2013).
Wickham, H. et al. Welcome to the Tidyverse. J. open source Softw. 4, 1686 (2019).
Douglas, G. M. et al. PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol. 38, 685–688 (2020).
pubmed: 32483366
pmcid: 7365738
Louca, S., Parfrey, L. W. & Doebeli, M. Decoupling function and taxonomy in the global ocean microbiome. Science 353, 1272–1277 (2016).
pubmed: 27634532
Boyd, J. A., Woodcroft, B. J. & Tyson, G. W. GraftM: a tool for scalable, phylogenetically informed classification of genes within metagenomes. Nucleic Acids Res. 46, e59 (2018).
pubmed: 29562347
pmcid: 6007438