The DOI matches its Crossref record; the references it cites are not checked yet.
Interkingdom interaction: the soil isopod Porcellio scaber stimulates the methane-driven bacterial and fungal interaction
Open accessAbstract
Porcellio scaber (woodlice) are (sub-)surface-dwelling isopods, widely recognized as “soil bioengineers”, modifying the edaphic properties of their habitat, and affecting carbon and nitrogen mineralization that leads to greenhouse gas emissions. Yet, the impact of soil isopods on methane-cycling processes remains unknown. Using P. scaber as a model macroinvertebrate in a microcosm study, we determined how the isopod influences methane uptake and the associated interaction network in an agricultural soil. Stable isotope probing (SIP) with 13C-methane was combined to a co-occurrence network analysis to directly link activity to the methane-oxidizing community (bacteria and fungus) involved in the trophic interaction. Compared to microcosms without the isopod, P. scaber significantly induced methane uptake, associated to a more complex bacteria-bacteria and bacteria-fungi interaction, and modified the soil nutritional status. Interestingly, 13C was transferred via the methanotrophs into the fungi, concomitant to significantly higher fungal abundance in the P. scaber-impacted soil, indicating that the fungal community utilized methane-derived substrates in the food web along with bacteria. Taken together, results showed the relevance of P. scaber in modulating methanotrophic activity with implications for bacteria-fungus interaction.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
The citation lists haven’t been fetched yet
References 88 · Cited by 9
Research works printed but not linked: 87
- Coleman, 2008, From peds to paradoxes: Linkages between soil biota and their influences on ecological processes, Soil Biol Biochem, 40, 271, 10.1016/j.soilbio.2007.08.005 · DOI
- Ho, 2013, Termites facilitate methane oxidation and shape the methanotrophic community, Appl Environ Microbiol, 79, 7234, 10.1128/AEM.02785-13 · DOI
- Grandy, 2016, Beyond microbes: Are fauna the next frontier in soil biogeochemical models?, Soil Biol Biochem, 102, 40, 10.1016/j.soilbio.2016.08.008 · DOI
- Des Marteaux, 2020, Terrestrial Isopods Porcellio scaber and Oniscus asellus (Crustacea: Isopoda) Increase Bacterial Abundance and Modify Microbial Community Structure in Leaf Litter Microcosms: a Short-Term Decomposition Study, Microb Ecol, 80, 690, 10.1007/s00248-020-01527-4 · DOI · Paper page
- Scheu, 2005, Microorganisms in soils: roles in genesis and functions, 253, 10.1007/3-540-26609-7_12 · DOI
- Lubbers, 2020, Soil fauna diversity increases CO2 but suppresses N2O emissions from soil, Glob Change Biol, 26, 1886, 10.1111/gcb.14860 · DOI
- Zimmer, 2005, Do woodlice and earthworms interact synergistically in leaf litter decomposition?, Funct Ecol, 19, 7, 10.1111/j.0269-8463.2005.00926.x · DOI
- Lilleskov, 2005, Spore dispersal of a resupinate ectomycorrhizal fungus, Tomentella sublilacina, via soil food webs, Mycologia., 97, 762, 10.1080/15572536.2006.11832767 · DOI
- Nechitaylo, 2010, Effect of the earthworms Lumbricus terrestris and Aporrectodea caliginosa on bacterial diversity in soil, Microb Ecol, 59, 574, 10.1007/s00248-009-9604-y · DOI
- Crowther, 2011, Outcomes of fungal interactions are determined by soil invertebrate grazers, Ecol Lett, 14, 1134, 10.1111/j.1461-0248.2011.01682.x · DOI
- Crowther, 2011, Species-specific effects of soil fauna on fungal foraging and decomposition, Oecologia., 167, 535, 10.1007/s00442-011-2005-1 · DOI
- Dempsey, 2011, Earthworms increase the ratio of bacteria to fungi in northern hardwood forest soils, primarily by eliminating the organic horizon, Soil Biol Biochem, 43, 2135, 10.1016/j.soilbio.2011.06.017 · DOI
- Soong, 2016, Soil microarthropods support ecosystem productivity and soil C accrual: Evidence from a litter decomposition study in the tallgrass prairie, Soil Biol Biochem, 92, 230, 10.1016/j.soilbio.2015.10.014 · DOI
- Drake, 2006, Earthworms as a transient heaven for terrestrial denitrifying microbes: a review, Eng Life Sci, 6, 261, 10.1002/elsc.200620126 · DOI
- Postma-Blaauw, 2006, Earthworm species composition affects the soil bacterial community and net nitrogen mineralization, Pedobiologia., 50, 243, 10.1016/j.pedobi.2006.02.001 · DOI
- Héry, 2008, Effect of earthworms on the community structure of active methanotrophic bacteria in a landfill cover soil, ISME J, 2, 92, 10.1038/ismej.2007.66 · DOI
- Nebert, 2011, Association of earthworm-denitrifier interactions with increased emission of nitrous oxide from soil mesocosms amended with crop residue, Appl Environ Microbiol, 77, 4097, 10.1128/AEM.00033-11 · DOI
- Slabber, 2002, The first record of a terrestrial crustacean, Porcellio scaber (Isopoda, Porcellionidae), from sub-Antarctic Marion Island, Polar Biol, 25, 855, 10.1007/s00300-002-0420-9 · DOI
- Hassal, 1977, Consumption of leaf litter by the terrestrial isopod Philoscia muscorum in relation to food availability in a dune grassland ecosystem, Ecol Bull, 25, 550
- Hink, 2023, Microplastic ingestion affects hydrogen production and microbiomes in the gut of the terrestrial isopod Porcellio scaber, 10.1111/1462-2920.16386 · DOI
- Knief, 2015, Diversity and habitat preferences of cultivated and uncultivated aerobic methanotrophic bacteria evaluated based on pmoA as molecular marker, Front Microbiol, 6, 1346, 10.3389/fmicb.2015.01346 · DOI
- Guerrero-Cruz, 2021, Methanotrophs: discoveries, environmental relevance, and a perspective on current and future applications, Front Microbiol, 12, 678057, 10.3389/fmicb.2021.678057 · DOI
- van Spanning, 2022, Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem, Nat Microbiol, 7, 2089, 10.1038/s41564-022-01252-3 · DOI
- Kaupper, 2021, Recovery in methanotrophic activity does not reflect on the methane-driven interaction network after peat mining, Appl Environ Microbiol, 87, e02355, 10.1128/AEM.02355-20 · DOI
- Schmitz, 2021, Verrucomicrobial methanotrophs: ecophysiology of metabolically versatile acidophiles, FEMS Microbiol Rev, 45, fuab007, 10.1093/femsre/fuab007 · DOI
- Reim, 2012, One millimetre makes the difference: high-resolution analysis of methane-oxidizing bacteria and their specific activity at the oxic-anoxic interface in a flooded paddy soil, ISME J, 6, 2128, 10.1038/ismej.2012.57 · DOI
- Praeg, 2017, Plant species, temperature, and bedrock affect net methane flux out of grassland and forest soils, Plant Soil, 410, 193, 10.1007/s11104-016-2993-z · DOI
- Kaupper, 2022, The methane-driven interaction network in terrestrial methane hotspots, Environ Microbiome, 17, 15, 10.1186/s40793-022-00409-1 · DOI
- Trotsenko, 2008, Metabolic aspects of aerobic obligate methanotrophy, Adv Appl Microbiol, 63, 183, 10.1016/S0065-2164(07)00005-6 · DOI
- Ho, 2017, Revisiting life strategy concepts in environmental microbial ecology, FEMS Microbiol Ecol, 93, 1
- Ho, 2013, Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies, Environ Microbiol Rep, 5, 335, 10.1111/j.1758-2229.2012.00370.x · DOI
- Semrau, 2018, Metals and methanotrophy, Appl Environ Microbiol, 84, e02289, 10.1128/AEM.02289-17 · DOI
- Scheu, 2002, Effects of the presence and community composition of earthworms on microbial community functioning, Oecologia., 133, 254, 10.1007/s00442-002-1023-4 · DOI
- Seeber, 2006, Effects of macro-decomposers on litter decomposition and soil properties in alpine pastureland: A mesocosm experiment, Appl Soil Ecol, 34, 168, 10.1016/j.apsoil.2006.02.004 · DOI
- Wu, 2015, Interactions between earthworms and mesofauna has no significant effect on emissions of CO2 and N2O from soil, Soil Biol Biochem, 88, 294, 10.1016/j.soilbio.2015.06.005 · DOI
- Chang, 2017, Amynthas agrestis invasion increases microbial biomass in Mid-Atlantic deciduous forests, Soil Biol Biochem, 114, 189, 10.1016/j.soilbio.2017.07.018 · DOI
- Ho, 2016, Biotic interactions in microbial communities as modulators of biogeochemical processes: methanotrophy as a model system, Front Microbiol, 7, 1285, 10.3389/fmicb.2016.01285 · DOI
- Kaupper, 2021, When the going gets tough: Emergence of a complex methane-driven interaction network during recovery from desiccation-rewetting, Soil Biol Biochem, 153, 108109, 10.1016/j.soilbio.2020.108109 · DOI
- Ho, 2015, Unexpected stimulation of soil methane uptake as emergent property of agricultural soils following bio-based residue application, Glob Change Biol, 21, 3864, 10.1111/gcb.12974 · DOI
- Ho, 2019, Unexpected role of canonical aerobic methanotrophs in upland agricultural soils, Soil Biol Biochem, 131, 1, 10.1016/j.soilbio.2018.12.020 · DOI
- Kaupper, 2020, Disentangling abiotic and biotic controls of aerobic methane oxidation during re-colonization, Soil Biol Biochem, 142, 107729, 10.1016/j.soilbio.2020.107729 · DOI
- Ho, 2017, Effects of bio-based residue amendments on greenhouse gas emission from agricultural soil are stronger than effects of soil type with different microbial community composition, Glob Change Biol Bioenergy, 9, 1707, 10.1111/gcbb.12457 · DOI
- El-Hawwary, 2022, Greenhouse gas (CO2, CH4, and N2O) emissions after abandonment of agriculture, Biol Fertil Soils, 58, 579, 10.1007/s00374-022-01644-x · DOI
- Hopkin, 1994, Zinc, among a ‘cocktail’ of metal pollutants, is responsible for the absence of the terrestrial isopod Porcellio scaber from the vicinity of a primary smelting works, Ecotoxicol, 3, 68, 10.1007/BF00121389 · DOI
- Brockett, 2005, The existence of an Allee effect in populations of Porcellio scaber (Isopoda: Oniscidea), Eur J Soil Biol, 41, 123, 10.1016/j.ejsobi.2005.09.004 · DOI
- Ho, 2011, Recovery of methanotrophs from disturbance: population dynamics, evenness and functioning, ISME J., 5, 750, 10.1038/ismej.2010.163 · DOI
- Zaman, 2021, Measuring emission of agricultural greenhouse gases and developing mitigation options using nuclear and related techniques, 109, 10.1007/978-3-030-55396-8_3 · DOI
- van Dijk, 2021, Discrepancy in exchangeable and soluble ammonium-induced effects on aerobic methane oxidation: a microcosm study of a paddy soil, Biol Fertil Soils, 57, 873, 10.1007/s00374-021-01579-9 · DOI
- Horn, 2005, Dechloromonas denitrificans sp. nov., Flavobacterium denitrificans sp. nov., Paenibacillus anaericanus sp. nov. and Paenibacillus terrae strain MH72, N2O-producing bacteria isolated from the gut of the earthworm Aporrectodea caliginosa, Int J Syst Evol Microbiol, 55, 1255, 10.1099/ijs.0.63484-0 · DOI
- Griffiths, 2000, Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition, Appl Environ Microbiol, 66, 5488, 10.1128/AEM.66.12.5488-5491.2000 · DOI
- Hetz, 2021, Burkholderiaceae are key acetate assimilators during complete denitrification in acidic cryoturbated peat circles of the arctic tundra, Front Microbiol, 12, 628269, 10.3389/fmicb.2021.628269 · DOI
- Neufeld, 2007, DNA stable-isotope probing, Nat Protoc, 2, 860, 10.1038/nprot.2007.109 · DOI
- Ho, 2020, Response of a methane-driven interaction network to stressor intensification, FEMS Microbiol Ecol, 96, fiaa180, 10.1093/femsec/fiaa180 · DOI
- Zhang, 2014, PEAR: a fast and accurate Illumina Paired-End reAd mergeR, Bioinformatics., 30, 614, 10.1093/bioinformatics/btt593 · DOI · Paper page
- Callahan, 2016, DADA2: High-resolution sample inference from Illumina amplicon data, Nat Methods, 13, 581, 10.1038/nmeth.3869 · DOI · Paper page
- Quast, 2013, The SILVA ribosomal RNA gene database project: improved data processing and web-based tools, Nucleic Acids Res, 41, D590, 10.1093/nar/gks1219 · DOI · Paper page
- Nilsson, 2019, The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications, Nucleic Acids Res, 47, D259, 10.1093/nar/gky1022 · DOI
- Anderson, 2001, A new method for non-parametric multivariate analysis of variance, Austral Ecol, 26, 32
- Hammer, 2001, PAST: Paleontological statistics software package for education and data analysis: Palaeontol Electron
- Friedman, 2012, Inferring correlation networks from genomic survey data, PLOS Comput Biol, 8, e1002687, 10.1371/journal.pcbi.1002687 · DOI
- Bastian, 2009, Gephi: an open source software for exploring and manipulating networks, ICWSM Conf, 3, 361, 10.1609/icwsm.v3i1.13937 · DOI · Paper page
- Borgatti, 2005, Centrality and network flow, Soc Netw, 27, 55, 10.1016/j.socnet.2004.11.008 · DOI · Paper page
- Poudel, 2016, Microbiome networks: a systems framework for identifying candidate microbial assemblages for disease management, Phytopathology., 106, 1083, 10.1094/PHYTO-02-16-0058-FI · DOI
- Maurer, 2008, Inhibition of atmospheric methane oxidation by monoterpenes in Norway spruce and European beech soils, Soil Biol Biochem, 40, 3014, 10.1016/j.soilbio.2008.08.023 · DOI
- Amaral, 1998, Effect of selected monoterpenes on methane oxidation, denitrification, and aerobic metabolism by bacteria in pure culture, Appl Environ Microbiol, 64, 520, 10.1128/AEM.64.2.520-525.1998 · DOI
- Bray, 2019, Soil macroinvertebrate presence alters microbial community composition and activity in the rhizosphere, Front Microbiol, 10, 256, 10.3389/fmicb.2019.00256 · DOI
- Liu, 2013, Consumers of 4-chloro-2-methylphenoxyacetic acid from agricultural soil and drilosphere harbor cadA, r/sdpA, and tfdA-like gene encoding oxygenases, FEMS Microbiol Ecol, 86, 114, 10.1111/1574-6941.12144 · DOI
- Liu, 2011, The earthworm Aporrectodea caliginosa stimulates abundance and activity of phenoxyalkanoic acid herbicide degraders, ISME J., 5, 473, 10.1038/ismej.2010.140 · DOI
- Dallinger, 2014, Agricultural soil and drilosphere as reservoirs of new and unusual assimilators of 2,4-dichlorophenol carbon, Environ Microbiol, 16, 84, 10.1111/1462-2920.12209 · DOI
- Alam, 2012, Inhibition of methane oxidation by nitrogenous fertilizers in a paddy soil, Front Microbiol, 3, 246, 10.3389/fmicb.2012.00246 · DOI
- López, 2019, Ammonium influences kinetics and structure of methanotrophic consortia, Waste manag, 89, 345, 10.1016/j.wasman.2019.04.028 · DOI
- Maraun, 2003, Adding to ‘the enigma of soil animal diversity’: fungal feeders and saprophagous soil invertebrates prefer similar food substrates, Eur J Soil Biol, 39, 85, 10.1016/S1164-5563(03)00006-2 · DOI
- Ihnen, 2008, Selective consumption and digestion of litter microbes by Porcellio scaber (Isopoda: Oniscidea), Pedobiologia., 51, 335, 10.1016/j.pedobi.2007.06.001 · DOI · Paper page
- Six, 2000, Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture, Soil Biol Biochem, 32, 2099, 10.1016/S0038-0717(00)00179-6 · DOI · Paper page
- McTiernan, 1997, Respiration and Nutrient Release from Tree Leaf Litter Mixtures, Oikos., 78, 527, 10.2307/3545614 · DOI
- Warmink, 2011, Hitchhikers on the fungal highway: The helper effect for bacterial migration via fungal hyphae, Soil Biol Biochem, 43, 760, 10.1016/j.soilbio.2010.12.009 · DOI
- Worrich, 2017, Mycelium-mediated transfer of water and nutrients stimulates bacterial activity in dry and oligotrophic environments, Nat Commun, 8, 15472, 10.1038/ncomms15472 · DOI
- Dedysh, 2002, Methylocapsa acidiphila gen. nov., sp. nov., a novel methane-oxidizing and dinitrogen-fixing acidophilic bacterium from Sphagnum bog, Int J Syst Evol Microbiol, 52, 251, 10.1099/00207713-52-1-251 · DOI
- De Boer, 2008, Interactions between saprotrophic basidiomycetes and bacteria, Br Mycol Soc Symp Ser, 28, 143
- Ho, 2014, The more, the merrier: heterotroph richness stimulates methanotrophic activity, ISME J., 8, 1945, 10.1038/ismej.2014.74 · DOI
- Veraart, 2018, Living apart together-bacterial volatiles influence methanotrophic growth and activity, ISME J, 12, 1163, 10.1038/s41396-018-0055-7 · DOI
- van der Heijden, 2016, Networking in the plant microbiome, PLOS Biol, 14, e1002378, 10.1371/journal.pbio.1002378 · DOI
- Shi, 2020, Novel synergistic mechanism for lignocellulose degradation by a thermophilic filamentous fungus and a thermophilic actinobacterium based on functional proteomics, Front Microbiol, 11, 539438, 10.3389/fmicb.2020.539438 · DOI
- Singh, 2003, Thermomyces lanuginosus: properties of strains and their hemicellulases, FEMS Microbiol Rev, 27, 3, 10.1016/S0168-6445(03)00018-4 · DOI
- James, 2016, Apiotrichum terrigenum sp. nov., a soil-associated yeast found in both the UK and mainland Europe, Int J Syst and Evol Microbiol, 66, 5046, 10.1099/ijsem.0.001467 · DOI
- Veen, 2021, Steering the soil microbiome by repeated litter addition, J Ecol, 109, 2499, 10.1111/1365-2745.13662 · DOI
- Pan, 2014, Remarkable recovery and colonization behaviour of methane oxidizing bacteria in soil after disturbance is controlled by methane source only, Microb Ecol, 68, 259, 10.1007/s00248-014-0402-9 · DOI
Metadata
- Authors
- Heffner, T., Brami, S. A., Mendes, L. W., Kaupper, T., Hannula, E. S., Poehlein, A., Horn, M. A., & Ho, A.
- Affiliations
- Leibniz University Hannover (DE)
- Universidade de São Paulo (BR)
- Leiden University, Department of Environmental Biology, Institute of Environmental Sciences , Einsteinweg 2, 2333CC Leiden, the Netherlands
- University of Göttingen (DE)
- Corresponding author
- Horn, Marcus A
- Ho, Adrian
- ORCID
- Venue
- ISME Communications
- Publisher
- Oxford University Press (OUP)
- Published
- 2023-06-24
- Volume
- 3
- Issue
- 1
- Pages
- 62-62
- ISSN
- 2730-6151 (ISSN-L)
- PMC
- PMC10290665
- OpenAlex
- W4381929523
- Cited by
- 9
- References
- 88
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 3
- FWCI
- 1.34
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- ISME Communications (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Leiden Repository (Leiden University) (submittedVersion, cc-by)
- Institutional Repository of Leibniz Universität Hannover (Leibniz Universität Hannover) (submittedVersion, cc-by)
- GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
- Institutional Repository of Leibniz Universität Hannover (Leibniz Universität Hannover) (submittedVersion, cc-by-nc-nd)
- Leibniz Universität Hannover (cc-by)
- Funders
- Deutsche Forschungsgemeinschaft (HO6234/1-2)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil Carbon and Nitrogen Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
- Physical Sciences › Environmental Science › Environmental Chemistry › Methane Hydrates and Related Phenomena
- Keywords
- Porcellio scaber, terrestrial isopods, methane uptake, methanotrophic bacteria, fungal-bacterial interactions, soil microbial communities, soil bioengineering, trophic interactions, co-occurrence network analysis, agricultural soils, soil carbon cycling, greenhouse gas emissions
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review