in

Habitat geometry in artificial microstructure affects bacterial and fungal growth, interactions, and substrate degradation

  • 1.

    IPCC, Working Group I Contribution to the IPCC Fifth Assessment Report, Climate Change 2013: The Physical Science Basis, AR5. 2013.

  • 2.

    IPCC, Working Group I Report ‘The Physical Science Basis,’ PCC Fourth Assessment Report. 2007.

  • 3.

    IPCC, “IPCC Fourth Assessment Report (AR4),” IPCC, 1, 976, 2007.

  • 4.

    Guerra, C. A. et al. Blind spots in global soil biodiversity and ecosystem function research. Nature Communications 11, 1–13 (2020).

    Article 
    CAS 

    Google Scholar 

  • 5.

    Nagy, K., Ábrahám, Á., Keymer, J. E. & Galajda, P. Application of microfluidics in experimental ecology: the importance of being spatial. Front. Microbiol. 9, 496 (2018).

  • 6.

    Tecon, R. & Or, D. Biophysical processes supporting the diversity of microbial life in soil. FEMS Microbiol. Rev. 41, 599–623 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 7.

    Falkowski, P. G., Fenchel, T. & Delong, E. F. The microbial engines that drive earth’s biogeochemical cycles. Science. https://doi.org/10.1126/science.1153213 (2008).

  • 8.

    Hobbie, J. E. & Hobbie, E. A. Microbes in nature are limited by carbon and energy: the starving-survival lifestyle in soil and consequences for estimating microbial rates. Front. Microbiol. 4, 1–11 (2013). no. NOV.

    Article 

    Google Scholar 

  • 9.

    Hill, P. W., Farrar, J. F. & Jones, D. L. Decoupling of microbial glucose uptake and mineralization in soil. Soil Biol. Biochem. https://doi.org/10.1016/j.soilbio.2007.09.008 (2008).

  • 10.

    IPCC. Climate change 2007: the physical science basis. 2007, https://doi.org/10.1260/095830507781076194.

  • 11.

    Baveye, P. C. et al. Emergent properties of microbial activity in heterogeneous soil microenvironments: different research approaches are slowly converging, yet major challenges remain. Front. Microbiol. https://doi.org/10.3389/fmicb.2018.01929 (2018).

  • 12.

    Bruand, A. & Cousin, I. Variation of textural porosity of a clay‐loam soil during compaction. Eur. J. Soil Sci. https://doi.org/10.1111/j.1365-2389.1995.tb01334.x (1995).

  • 13.

    Cnudde, V. & Boone, M. N. High-resolution X-ray computed tomography in geosciences: a review of the current technology and applications. Earth-Science Rev. https://doi.org/10.1016/j.earscirev.2013.04.003 (2013).

  • 14.

    Pagliai, M., Vignozzi, N. & Pellegrini, S. Soil structure and the effect of management practices. https://doi.org/10.1016/j.still.2004.07.002 (2004).

  • 15.

    Pires, L. F., Bacchi, O. O. S., Reichardt, K. & Timm, L. C. Application of γ-ray computed tomography to analysis of soil structure before density evaluations. Appl. Radiat. Isot. https://doi.org/10.1016/j.apradiso.2005.03.019 (2005).

  • 16.

    Larsbo, M., Koestel, J., Kätterer, T. & Jarvis, N. Preferential transport in macropores is reduced by soil organic carbon. Vadose Zone J. https://doi.org/10.2136/vzj2016.03.0021 (2016).

  • 17.

    Ananyeva, K., Wang, W., Smucker, A. J. M., Rivers, M. L. & Kravchenko, A. N. Can intra-aggregate pore structures affect the aggregate’s effectiveness in protecting carbon? Soil Biol. Biochem. https://doi.org/10.1016/j.soilbio.2012.10.019 (2013).

  • 18.

    Toosi, E. R., Kravchenko, A. N., Mao, J., Quigley, M. Y. & Rivers, M. L. Effects of management and pore characteristics on organic matter composition of macroaggregates: evidence from characterization of organic matter and imaging. Eur. J. Soil Sci. https://doi.org/10.1111/ejss.12411 (2017).

  • 19.

    Katuwal, S. et al. Linking air and water transport in intact soils to macropore characteristics inferred from X-ray computed tomography. Geoderma. https://doi.org/10.1016/j.geoderma.2014.08.006 (2015).

  • 20.

    Negassa, W. C. et al. Properties of soil pore space regulate pathways of plant residue decomposition and community structure of associated bacteria. PLoS ONE https://doi.org/10.1371/journal.pone.0123999 (2015).

  • 21.

    Rabot, E., Wiesmeier, M., Schlüter, S. & Vogel, H. J. Soil structure as an indicator of soil functions: a review. Geoderma. https://doi.org/10.1016/j.geoderma.2017.11.009 (2018).

  • 22.

    Pronk, G. J. et al. Interaction of minerals, organic matter, and microorganisms during biogeochemical interface formation as shown by a series of artificial soil experiments. Biol. Fertil. Soils. https://doi.org/10.1007/s00374-016-1161-1 (2017).

  • 23.

    Downie, H. et al. Transparent Soil for Imaging the Rhizosphere. PLoS ONE. https://doi.org/10.1371/journal.pone.0044276 (2012).

  • 24.

    Aleklett, K. et al. Build your own soil: exploring microfluidics to create microbial habitat structures. ISME J. 12, 312–319 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 25.

    Beebe, D. J., Mensing, G. A. & Walker, G. M. Physics and Applications of Microfluidics in Biology. Annu. Rev. Biomed. Eng. https://doi.org/10.1146/annurev.bioeng.4.112601.125916 (2002).

  • 26.

    Ahmed, T., Shimizu, T. S. & Stocker, R. Microfluidics for bacterial chemotaxis. Integr. Biol. https://doi.org/10.1039/c0ib00049c (2010).

  • 27.

    Ahmed, T. & Stocker, R. Experimental verification of the behavioral foundation of bacterial transport parameters using microfluidics. Biophys. J. https://doi.org/10.1529/biophysj.108.134510 (2008).

  • 28.

    Mao, H., Cremer, P. S. & Manson, M. D. A sensitive, versatile microfluidic assay for bacterial chemotaxis. Proc. Natl Acad. Sci. https://doi.org/10.1073/pnas.0931258100 (2003).

  • 29.

    Saragosti, J. et al. Directional persistence of chemotactic bacteria in a traveling concentration wave. Proc. Natl Acad. Sci. https://doi.org/10.1073/pnas.1101996108 (2011).

  • 30.

    Deng, J. et al. Synergistic effects of soil microstructure and bacterial EPS on drying rate in emulated soil micromodels. Soil Biol. Biochem. 83, 116–124 (2015).

    CAS 
    Article 

    Google Scholar 

  • 31.

    Rubinstein, R. L., Kadilak, A. L., Cousens, V. C., Gage, D. J. & Shor, L. M. Protist-facilitated particle transport using emulated soil micromodels. Environ. Sci. Technol. 49, 1384–1391 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 32.

    Stanley, C. E. et al. Probing bacterial-fungal interactions at the single cell level. Integr. Biol. 6, 935–945 (2014).

    CAS 
    Article 

    Google Scholar 

  • 33.

    Aleklett, K., Ohlsson, P., Bengtsson, M. & Hammer, E. C. Fungal foraging behaviour and hyphal space exploration in micro-structured Soil Chips. ISME J. https://doi.org/10.1038/s41396-020-00886-7 (2021).

  • 34.

    Mafla-Endara, P. M. et al. Microfluidic chips provide visual access to in situ soil ecology. Commun. Biol. 4, 889 (2021).

  • 35.

    Falconer, R., Houston, A., Otten, W. & Baveye, P. Emergent behavior of soil fungal dynamics: influence of soil architecture and water distribution. Soil Sci. 177, 111–119 (2012).

    CAS 
    Article 

    Google Scholar 

  • 36.

    Duffy, K. J. & Ford, R. M. Turn angle and run time distributions characterize swimming behavior for Pseudomonas putida. J. Bacteriol. 179, 1428–1430 (1997).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 37.

    Rashid, S. et al. Adjustment in tumbling rates improves bacterial chemotaxis on obstacle-laden terrains. Proc. Natl Acad Sci USA 116, 11770–11775 (2019).

  • 38.

    Duffy, K. J., Cummings, P. T. & Ford, R. M. Random walk calculations for bacterial migration in porous media. Biophys. J. 68, 800–806 (1995).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 39.

    Shum, H. & Gaffney, E. A. Hydrodynamic analysis of flagellated bacteria swimming in corners of rectangular channels. Phys. Rev. E 92, 1–11 (2015).

    Article 
    CAS 

    Google Scholar 

  • 40.

    Guadayol, Ò., Thornton, K. L. & Humphries, S. Cell morphology governs directional control in swimming bacteria. Sci. Rep. https://doi.org/10.1038/s41598-017-01565-y (2017).

  • 41.

    Essig, A. et al. Copsin, a novel peptide-based fungal antibiotic interfering with the peptidoglycan synthesis. J. Biol. Chem. 289, 34953–34964 (2014).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 42.

    Dixon, E. F. & Hall, R. A. Noisy neighbourhoods: quorum sensing in fungal-polymicrobial infections. Cell. Microbiol. 17, 1431–1441 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 43.

    Banitz, T. et al. Assessing biodegradation benefits from dispersal networks. Ecol. Model. 222, 2552–2560 (2011).

    Article 

    Google Scholar 

  • 44.

    Furuno, S. et al. Fungal mycelia allow chemotactic dispersal of polycyclic aromatic hydrocarbon-degrading bacteria in water-unsaturated systems. Environ. Microbiol. 12, 1391–1398 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 45.

    Kohlmeier, S. et al. Taking the fungal highway: mobilization of pollutant-degrading bacteria by fungi. Environ. Sci. Technol. 39, 4640–4646 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 46.

    Held, M., Kaspar, O., Edwards, C. & Nicolau, D. V. Intracellular mechanisms of fungal space searching in microenvironments. Proc. Natl Acad. Sci. USA 116, 13543–13552 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 47.

    Soufan, R. et al. Pore-scale monitoring of the effect of microarchitecture on fungal growth in a two-dimensional soil-like micromodel. Front. Environ. Sci. https://doi.org/10.3389/fenvs.2018.00068 (2018).

  • 48.

    Hanson, K. L. et al. Fungi use efficient algorithms for the exploration of microfluidic networks. Small 2, 1212–1220 (2006).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 49.

    Pajor, R., Falconer, R., Hapca, S. & Otten, W. Modelling and quantifying the effect of heterogeneity in soil physical conditions on fungal growth. Biogeosciences 7, 3731–3740 (2010).

    Article 

    Google Scholar 

  • 50.

    Varma, A., Abbott, L., Werner, D. & Hampp, R. Plant Surface Microbiology (Springer, 2008)..

  • 51.

    Lew, R. R. How does a hypha grow? The biophysics of pressurized growth in fungi. Nat. Rev. Microbiol. 9, 509–518 (2011).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 52.

    Tayagui, A., Sun, Y., Collings, D. A., Garrill, A. & Nock, V. An elastomeric micropillar platform for the study of protrusive forces in hyphal invasion. Lab a Chip 17, 3643–3653 (2017).

    CAS 
    Article 

    Google Scholar 

  • 53.

    Bardgett, R. D. & McAlister, E. The measurement of soil fungal:bacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands. Biol. Fertil. Soils 29, 282–290 (1999).

    Article 

    Google Scholar 

  • 54.

    De Deyn, G. B., Cornelissen, J. H. C. & Bardgett, R. D. Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol. Lett. 11, 516–531 (2008).

    PubMed 
    Article 

    Google Scholar 

  • 55.

    Kuijper, L. D. J., Berg, M. P., Morriën, E., Kooi, B. W. & Verhoef, H. A. Global change effects on a mechanistic decomposer food web model. Glob. Change Biol. 11, 249–265 (2005).

    Article 

    Google Scholar 

  • 56.

    Falconer, R. E. et al. Microscale heterogeneity explains experimental variability and non-linearity in soil organic matter mineralisation. PLoS ONE 10, e0123774 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 57.

    Deveau, A. et al. Bacterial-fungal interactions: ecology, mechanisms and challenges. FEMS Microbiol. Rev. 42, 335–352 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 58.

    Postma, J. & van Veen, J.A. Habitable pore space and survival of Rhizobium leguminosarum biovar trifolii introduced into soil. Microb. Ecol. 19, 149–161 (1990).

  • 59.

    Grundmann, G. L. Spatial scales of soil bacterial diversity—the size of a clone. FEMS Microbiol. Ecol. 48, 119–127 (2004).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 60.

    Kuzyakov, Y. & Blagodatskaya, E. Microbial hotspots and hot moments in soil: concept & review. Soil Biol. Biochem. 83, 184–199 (2015).

    CAS 
    Article 

    Google Scholar 

  • 61.

    Kim, D. S. & Fogler, H. S. Biomass evolution in porous media and its effects on permeability under starvation conditions. Biotechnol. Bioeng. 69, 47–56 (2000).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 62.

    Dupin, H. J. & McCarty, P. L. Mesoscale and microscale observations of biological growth in a silicon pore imaging element. Environ. Sci. Technol. 33, 1230–1236 (1999).

    CAS 
    Article 

    Google Scholar 

  • 63.

    Aufrecht, J. A. et al. Pore-scale hydrodynamics influence the spatial evolution of bacterial biofilms in a microfluidic porous network. PLoS ONE 14, 1–17 (2019).

    Article 
    CAS 

    Google Scholar 

  • 64.

    Vervoort, R. W. & Cattle, S. R. Linking hydraulic conductivity and tortuosity parameters to pore space geometry and pore-size distribution. J. Hydrol. 272, 36–49 (2003).

    Article 

    Google Scholar 

  • 65.

    Kögel-Knabner, I. The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol. Biochem. 34, 139–162 (2002).

    Article 

    Google Scholar 

  • 66.

    Hoffman, M. T. & Arnold, A. E. Diverse bacteria inhabit living hyphae of phylogenetically diverse fungal endophytes. Appl. Environ. Microbiol. 76, 4063–4075 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 67.

    Thompson, L. R. et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature 551, 457–463 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 68.

    Mcdonald, J. C., Duffy, D. C., Anderson, J. R. & Chiu, D. T. Review general fabrication of microfluidic systems in poly (dimethylsiloxane). Electrophoresis 21, 27–40 (2000).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 69.

    Cánovas, D., Cases, I. & De Lorenzo, V. Heavy metal tolerance and metal homeostasis in Pseudomonas putida as revealed by complete genome analysis. Environ. Microbiol. 5, 1242–1256 (2003).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 70.

    Mooney, A., Ward, P. G. & O’Connor, K. E. Microbial degradation of styrene: biochemistry, molecular genetics, and perspectives for biotechnological applications. Appl. Microbiol. Biotechnol. 72, 1–10 (2006).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 71.

    Ward, P. G., Goff, M., Donner, M., Kaminsky, W. & O’Connor, K. E. A two step chemo-biotechnological conversion of polystyrene to a biodegradable thermoplastic. Environ. Sci. Technol. 40, 2433–2437 (2006).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 72.

    Gomes, N. C. M., Kosheleva, I. A., Abraham, W. R. & Smalla, K. Effects of the inoculant strain Pseudomonas putida KT2442 (pNF142) and of naphthalene contamination on the soil bacterial community. FEMS Microbiol. Ecol. 54, 21–33 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 73.

    Smith, M. C. M. Molecular biological methods for bacillus. FEBS Lett. https://doi.org/10.1016/0014-5793(91)80059-c. (1991).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 74.

    Razavi, B. S., Zhang, X., Bilyera, N., Guber, A. & Zarebanadkouki, M. Soil zymography: simple and reliable? Review of current knowledge and optimization of the method. Rhizosphere 11, 100161 (2019). no. June.

    Article 

    Google Scholar 

  • 75.

    Nicodème, M., Grill, J. P., Humbert, G. & Gaillard, J. L. Extracellular protease activity of different Pseudomonas strains: dependence of proteolytic activity on culture conditions. J. Appl. Microbiol. https://doi.org/10.1111/j.1365-2672.2005.02634.x (2005).

  • 76.

    Güll, I., Alves, P. M., Gabor, F. & Wirth, M. Viability of the human adenocarcinoma cell line Caco-2: influence of cryoprotectant, freezing rate, and storage temperature. Scientia Pharmaceutica https://doi.org/10.3797/scipharm.0810-07 (2009).

  • 77.

    Burns, C. et al. Efficient GFP expression in the mushrooms Agaricus bisporus and Coprinus cinereus requires introns. Fungal Genetics Biol. https://doi.org/10.1016/j.fgb.2004.11.005 (2005).

  • 78.

    Stajich, J. E. et al. Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc. Natl Acad. Sci. USA 107, 11889–11894 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 79.

    Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods. https://doi.org/10.1038/nmeth.2019 (2012).

  • 80.

    Kneen, M. A. & Annegarn, H. J. Algorithm for fitting XRF, SEM and PIXE X-ray spectra backgrounds. Nucl. Instrum. Methods Phys. Res. Section B https://doi.org/10.1016/0168-583X(95)00908-6 (1996).

  • 81.

    Team, R. C. R: a language and environment for statistical computing. Vienna, Austria, 2019.

  • 82.

    Dunn, O. J. Multiple comparisons among means. J. Am. Stat. Assoc. https://doi.org/10.2307/2282330 (1961).

  • 83.

    Holm, S. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 1979.

  • 84.

    C. et al. Arellano-Caicedo, “Habitat geometry in artificial microstructure affects bacterial and fungal growth, interactions, and substrate degradation 2nd part,” Dryad, Dataset. 2021.

  • 85.

    C. et al. Arellano-Caicedo, “Habitat geometry in artificial microstructure affects bacterial and fungal growth, interactions, and substrate degradation. Part 1,” Dryad, Dataset, 2021.


  • Source: Ecology - nature.com

    Eat me, or don’t eat me?

    MIT Energy Initiative awards seven Seed Fund grants for early-stage energy research