Synchrotron radiation-based microcomputed tomography for three-dimensional growth analysis of Aspergillus niger pellets.
3D image analysis
Aspergillus niger
computed tomography
filamentous fungi
morphology
pellet growth
Journal
Biotechnology and bioengineering
ISSN: 1097-0290
Titre abrégé: Biotechnol Bioeng
Pays: United States
ID NLM: 7502021
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
05
05
2023
received:
01
03
2023
accepted:
11
07
2023
pubmed:
21
7
2023
medline:
21
7
2023
entrez:
21
7
2023
Statut:
ppublish
Résumé
Filamentous fungi produce a wide range of relevant biotechnological compounds. The close relationship between fungal morphology and productivity has led to a variety of analytical methods to quantify their macromorphology. Nevertheless, only a µ-computed tomography (µ-CT) based method allows a detailed analysis of the 3D micromorphology of fungal pellets. However, the low sample throughput of a laboratory µ-CT limits the tracking of the micromorphological evolution of a statistically representative number of submerged cultivated fungal pellets over time. To meet this challenge, we applied synchrotron radiation-based X-ray microtomography at the Deutsches Elektronen-Synchrotron [German Electron Synchrotron Research Center], resulting in 19,940 3D analyzed individual fungal pellets that were obtained from 26 sampling points during a 48 h Aspergillus niger submerged batch cultivation. For each of the pellets, we were able to determine micromorphological properties such as number and density of spores, tips, branching points, and hyphae. The computed data allowed us to monitor the growth of submerged cultivated fungal pellets in highly resolved 3D for the first time. The generated morphological database from synchrotron measurements can be used to understand, describe, and model the growth of filamentous fungal cultivations.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3244-3260Subventions
Organisme : Deutsche Forschungsgemeinschaft
Organisme : Deutsches Elektronen-Synchrotron
Organisme : Helmholtz Association
Organisme : Projekt DEAL
Organisme : SPP2170 InterZell-427889137
Organisme : SPP 1934 DiSPBiotech-315384307 and 315305620
Informations de copyright
© 2023 The Authors. Biotechnology and Bioengineering published by Wiley Periodicals LLC.
Références
Antimonov, M., Khounsary, A., Weigand, S., Rix, J., Keane, D., Grudzinski, J. J., & Jansma, W. (2015). Large-area Kapton X-ray windows (pp. 62-71). SPIE. https://doi.org/10.1117/12.2193680
Bishop, C. M. (2009). Pattern recognition and machine learning (Corrected at 8th printing 2009), Information science and statistics. Springer.
Buffo, M. M., Esperança, M. N., Farinas, C. S., & Badino, A. C. (2020). Relation between pellet fragmentation kinetics and cellulolytic enzymes production by Aspergillus niger in conventional bioreactor with different impellers. Enzyme and Microbial Technology, 139, 109587. https://doi.org/10.1016/j.enzmictec.2020.109587
Buschulte, T. C. (1992). Mathematische Modellbildung und Simulation von Zellwachstum, Stofftransport und Stoffwechsel in Pellets aus Streptomyceten (PhD thesis). Fakultät Verfahrenstechnik der Universität Stuttgart.
Cairns, T. C., Feurstein, C., Zheng, X., Zheng, P., Sun, J., & Meyer, V. (2019). A quantitative image analysis pipeline for the characterization of filamentous fungal morphologies as a tool to uncover targets for morphology engineering: A case study using aplD in Aspergillus niger. Biotechnology for Biofuels, 12, 149. https://doi.org/10.1186/s13068-019-1473-0
Cairns, T. C., Nai, C., & Meyer, V. (2018). How a fungus shapes biotechnology: 100 years of Aspergillus niger research. Fungal Biology and Biotechnology, 5, 13. https://doi.org/10.1186/s40694-018-0054-5
Cairns, T. C., Zheng, X., Zheng, P., Sun, J., & Meyer, V. (2019). Moulding the mould: Understanding and reprogramming filamentous fungal growth and morphogenesis for next generation cell factories. Biotechnology for Biofuels, 12, 77. https://doi.org/10.1186/s13068-019-1400-4
Caldwell, I. Y., & Trinci, A. P. J. (1973). The growth unit of the mould Geotrichum candidum. Archiv für Mikrobiologie, 88(1), 1-10.
Celler, K., Picioreanu, C., van Loosdrecht, M. C. M., & van Wezel, G. P. (2012). Structured morphological modeling as a framework for rational strain design of Streptomyces species. Antonie Van Leeuwenhoek, 102(3, SI), 409-423.
Colin, V. L., Baigorí, M. D., & Pera, L. M. (2013). Tailoring fungal morphology of Aspergillus niger MYA 135 by altering the hyphal morphology and the conidia adhesion capacity: Biotechnological applications. AMB Express, 3, 27.
Cui, Y. Q., Okkerse, W. J., van der Lans, R. G. J. M., & Luyben, K. C. A. M. (1998). Modeling and measurements of fungal growth and morphology in submerged fermentations. Biotechnology and Bioengineering, 60(2), 216-229.
Dynesen, J., & Nielsen, J. (2003). Branching is coordinated with mitosis in growing hyphae of Aspergillus nidulans. Fungal Genetics and Biology, 40(1), 15-24. https://doi.org/10.1016/S1087-1845(03)00053-7
Ehgartner, D., Herwig, C., & Fricke, J. (2017). Morphological analysis of the filamentous fungus Penicillium chrysogenum using flow cytometry-the fast alternative to microscopic image analysis. Applied Microbiology and Biotechnology, 101(20), 7675-7688.
El-Enshasy, H. A. (2011). Filamentous fungal cultures-Process characteristics, products, and applications. In S.-T. Yang (Ed.), Bioprocessing for value-added products from renewable resources: New technologies and applications (pp. 225-261). Elsevier Science. https://doi.org/10.1016/B978-044452114-9/50010-4
Ester, M., Kriegel, H.-P., Sander, J., & Xu, X. (1996). A density-based algorithm for discovering clusters in large spatial databases with noise. In Proceedings of the 2nd International conference on knowledge discovery and data mining, (Vol. 96, pp. 226-231).
Fiedler, M. R. M., Barthel, L., Kubisch, C., Nai, C., & Meyer, V. (2018). Construction of an improved Aspergillus niger platform for enhanced glucoamylase secretion. Microbial Cell Factories, 17(1), 95. https://doi.org/10.1186/s12934-018-0941-8
Füting, P., Barthel, L., Cairns, T. C., Briesen, H., & Schmideder, S. (2021). Filamentous fungal applications in biotechnology: A combined bibliometric and patentometric assessment. Fungal Biology and Biotechnology, 8(1), 23. https://doi.org/10.1186/s40694-021-00131-6
Glass, N. (2004). Hyphal homing, fusion and mycelial interconnectedness. Trends in Microbiology, 12(3), 135-141. https://doi.org/10.1016/j.tim.2004.01.007
Greving, I., Wilde, F., Ogurreck, M., Herzen, J., Hammel, J. U., Hipp, A., & Beckmann, F. (2014). P05 imaging beamline at PETRA III: First results. In S. R. Stock, (Ed.), SPIE proceedings, developments in X-ray tomography IX (92120O). SPIE. https://doi.org/10.1117/12.2061768
Günther, B., Gradl, R., Jud, C., Eggl, E., Huang, J., Kulpe, S., Achterhold, K., Gleich, B., Dierolf, M., & Pfeiffer, F. (2020). The versatile X-ray beamline of the Munich compact light source: Design, instrumentation and applications. Journal of Synchrotron Radiation, 27(5), 1395-1414. https://doi.org/10.1107/S1600577520008309
Haibel, A., Ogurreck, M., Beckmann, F., Dose, T., Wilde, F., Herzen, J., & Mohr, J. (2010). Micro- and nano-tomography at the GKSS Imaging Beamline at PETRA III. In S. R. Stock, (Ed.), SPIE proceedings, developments in X-ray tomography VII (78040B). SPIE. https://doi.org/10.1117/12.860852
Haralick, R. M., & Shapiro, L. G. (1992). Computer and robot vision (II). Addison-Wesley.
Hille, A., Neu, T. R., Hempel, D. C., & Horn, H. (2009). Effective diffusivities and mass fluxes in fungal biopellets. Biotechnology and Bioengineering, 103(6), 1202-1213.
Jacobson, A., & Panozzo, D. (2018). libigl: A simple C++ geometry processing library.
Kerschnitzki, M., Kollmannsberger, P., Burghammer, M., Duda, G. N., Weinkamer, R., Wagermaier, W., & Fratzl, P. (2013). Architecture of the osteocyte network correlates with bone material quality. Journal of Bone and Mineral Research, 28(8), 1837-1845. https://doi.org/10.1002/jbmr.1927
King, R. (1998). Mathematical modelling of the morphology of streptomyces species: Relation between morphology and process performances. In K. Schügerl, (Ed.), Relation between morphology and process performances (pp. 95-124). Springer Berlin Heidelberg.
King, R. (2015). A framework for an organelle-based mathematical modeling of hyphae. Fungal Biology and Biotechnology, 2(1), 5. https://doi.org/10.1186/s40694-015-0014-2
Kurt, T., Marbà-Ardébol, A.-M., Turan, Z., Neubauer, P., Junne, S., & Meyer, V. (2018). Rocking Aspergillus: Morphology-controlled cultivation of Aspergillus niger in a wave-mixed bioreactor for the production of secondary metabolites. Microbial Cell Factories, 17(1), 128. https://doi.org/10.1186/s12934-018-0975-y
Kurtz, S. M. (2012). PEEK biomaterials handbook. William Andrew Publishing.
Kwon, M. J., Nitsche, B. M., Arentshorst, M., Jørgensen, T. R., Ram, A. F. J., & Meyer, V. (2013). The transcriptomic signature of RacA activation and inactivation provides new insights into the morphogenetic network of Aspergillus niger. PLoS One, 8(7), e68946.
Lee, T. C., Kashyap, R. L., & Chu, C. N. (1994). Building skeleton models via 3-D medial surface axis thinning algorithms. CVGIP: Graphical Models and Image Processing, 56(6), 462-478. https://doi.org/10.1006/cgip.1994.1042
Lejeune, R., & Baron, G. V. (1997). Simulation of growth of a filamentous fungus in 3 dimensions. Biotechnology and Bioengineering, 53(2), 139-150.
Lewis, J. P. (1995). Fast normalized cross-correlation. In Vision Interface, 120-123.
Lytaev, P., Hipp, A., Lottermoser, L., Herzen, J., Greving, I., Khokhriakov, I., & Beckmann, F. (2014). Characterization of the CCD and CMOS cameras for grating-based phase-contrast tomography. In S. R. Stock, (Ed.), SPIE proceedings, developments in X-ray tomography IX (p. 921218). SPIE. https://doi.org/10.1117/12.2061389
Lyu, J., Tegelaar, M., Post, H., Moran Torres, J., Torchia, C., Altelaar, A. F. M., Bleichrodt, R. J., de Cock, H., Lugones, L. G., & Wösten, H. A. B. (2023). Heterogeneity in spore aggregation and germination results in different sized, cooperative microcolonies in an Aspergillus niger culture. mBio, 14(1), e0087022. https://doi.org/10.1128/mbio.00870-22
Maurer, C. R., Qi, R., & Raghavan, V. (2003). A linear time algorithm for computing exact Euclidean distance transforms of binary images in arbitrary dimensions. IEEE Transactions on Pattern Analysis and Machine Intelligence, 25(2), 265-270. https://doi.org/10.1109/TPAMI.2003.1177156
Meyer, F. (1994). Topographic distance and watershed lines. Signal processing, 38(1), 113-125. https://doi.org/10.1016/0165-1684(94)90060-4
Meyer, V., Basenko, E. Y., Benz, J. P., Braus, G. H., Caddick, M. X., Csukai, M., de Vries, R. P., Endy, D., Frisvad, J. C., Gunde-Cimerman, N., Haarmann, T., Hadar, Y., Hansen, K., Johnson, R. I., Keller, N. P., Kraševec, N., Mortensen, U. H., Perez, R., Ram, A. F. J., … Wösten, H. A. B. (2020). Growing a circular economy with fungal biotechnology: A white paper. Fungal Biology and Biotechnology, 7(1), 5. https://doi.org/10.1186/s40694-020-00095-z
Meyer, V., Cairns, T., Barthel, L., King, R., Kunz, P., Schmideder, S., Müller, H., Briesen, H., Dinius, A., & Krull, R. (2021). Understanding and controlling filamentous growth of fungal cell factories: Novel tools and opportunities for targeted morphology engineering. Fungal Biology and Biotechnology, 8(1), 8. https://doi.org/10.1186/s40694-021-00115-6
Meyer, V., Ram, A. F. J., & Punt, P. J. (2010). Genetics, genetic manipulation, and approaches to strain improvement of filamentous fungi. In R. H. Baltz, J. E. Davies, & A. L. Demain (Eds.), Reference manual, ASM Press. Manual of industrial microbiology and biotechnology (3rd ed., pp. 318-329). ASM Press. https://doi.org/10.1128/9781555816827.ch22
Moosmann, J., Ershov, A., Weinhardt, V., Baumbach, T., Prasad, M. S., LaBonne, C., Xiao, X., Kashef, J., & Hofmann, R. (2014). Time-lapse X-ray phase-contrast microtomography for in vivo imaging and analysis of morphogenesis. Nature Protocols, 9(2), 294-304. https://doi.org/10.1038/nprot.2014.033
Müller, H., Barthel, L., Schmideder, S., Schütze, T., Meyer, V., & Briesen, H. (2022). From spores to fungal pellets: A new high-throughput image analysis highlights the structural development of Aspergillus niger. Biotechnology and Bioengineering, 119(8), 2182-2195. https://doi.org/10.1002/bit.28124
Nielsen, J. (1996). Modelling the morphology of filamentous microorganisms. Trends in Biotechnology, 14(11), 438-443. https://doi.org/10.1016/0167-7799(96)10055-X
Nitsche, B. M., Burggraaf-van Welzen, A.-M., Lamers, G., Meyer, V., & Ram, A. F. J. (2013). Autophagy promotes survival in aging submerged cultures of the filamentous fungus Aspergillus niger. Applied Microbiology and Biotechnology, 97(18), 8205-8218. https://doi.org/10.1007/s00253-013-4971-1
Otsu, N. (1979). A threshold selection method from gray-level histograms. IEEE Transactions on Systems, Man and Cybernetics, 9, 62-66.
Palenstijn, W. J., Batenburg, K. J., & Sijbers, J. (2011). Performance improvements for iterative electron tomography reconstruction using graphics processing units (GPUs). Journal of Structural Biology, 176(2), 250-253. https://doi.org/10.1016/j.jsb.2011.07.017
Papagianni, M. (2004). Fungal morphology and metabolite production in submerged mycelial processes. Biotechnology Advances, 22(3), 189-259.
Papagianni, M., & Mattey, M. (2006). Morphological development of Aspergillus niger in submerged citric acid fermentation as a function of the spore inoculum level. Application of neural network and cluster analysis for characterization of mycelial morphology. Microbial Cell Factories, 5. https://doi.org/10.1186/1475-2859-5-3
Posch, A. E., Spadiut, O., & Herwig, C. (2012). A novel method for fast and statistically verified morphological characterization of filamentous fungi. Fungal Genetics and Biology, 49(7), 499-510.
Schmideder, S., Barthel, L., Friedrich, T., Thalhammer, M., Kovačević, T., Niessen, L., Meyer, V., & Briesen, H. (2019). An X-ray microtomography-based method for detailed analysis of the three-dimensional morphology of fungal pellets. Biotechnology and Bioengineering, 116(6), 1355-1365. https://doi.org/10.1002/bit.26956
Schmideder, S., Barthel, L., Müller, H., Meyer, V., & Briesen, H. (2019). From three-dimensional morphology to effective diffusivity in filamentous fungal pellets. Biotechnology and Bioengineering, 116(12), 3360-3371. https://doi.org/10.1002/bit.27166
Schmideder, S., Müller, H., Barthel, L., Friedrich, T., Niessen, L., Meyer, V., & Briesen, H. (2020). Universal law for diffusive mass transport through mycelial networks. Biotechnology and Bioengineering, 118(2), 930-943. https://doi.org/10.1002/bit.27622
Schuhmann, E., & Bergter, F. (1976). [Microscopic studies of Streptomyces hygroscopicus growth kinetics]. Zeitschrift fur Allgemeine Mikrobiologie, 16(3), 201-205. https://doi.org/10.1002/jobm.19760160305
Tegelaar, M., Aerts, D., Teertstra, W. R., & Wösten, H. A. B. (2020). Spatial induction of genes encoding secreted proteins in micro-colonies of Aspergillus niger. Scientific Reports, 10(1), 1536. https://doi.org/10.1038/s41598-020-58535-0
Thiry, M., Beckmann, F., Hammel, J. U., Moosmann, J. P., & Wilde, F. (2021). Brilliant light for materials science: Industrial applications of the high energy microtomography at beamline HEMS/P07 at PETRA III. In B. Müller & G. Wang, (Eds.), Proceedings of SPIE: Volume 11840, developments in X-ray tomography XIII: 1-5 August 2021, San Diego, California, United States (p. 20). SPIE. https://doi.org/10.1117/12.2596669
Trinci, A. P. (1974). A study of the kinetics of hyphal extension and branch initiation of fungal mycelia. Journal of General Microbiology, 81(1), 225-236.
Van Aarle, W., Palenstijn, W. J., De Beenhouwer, J., Altantzis, T., Bals, S., Batenburg, K. J., & Sijbers, J. (2015). The ASTRA toolbox: A platform for advanced algorithm development in electron tomography. Ultramicroscopy, 157, 35-47. https://doi.org/10.1016/j.ultramic.2015.05.002
Van Aarle, W., Palenstijn, W. J., Cant, J., Janssens, E., Bleichrodt, F., Dabravolski, A., De Beenhouwer, J., Joost Batenburg, K., & Sijbers, J. (2016). Fast and flexible X-ray tomography using the ASTRA toolbox. Optics Express, 24(22), 25129-25147. https://doi.org/10.1364/OE.24.025129
Veiter, L., Kubicek, M., Hutter, H., Pittenauer, E., Herwig, C., & Slouka, C. (2020). Study of metabolism and identification of productive regions in filamentous fungi via spatially resolved time-of-flight secondary ion mass spectrometry. Analytical and Bioanalytical Chemistry, 412(9), 2081-2088. https://doi.org/10.1007/s00216-019-01980-2
Veiter, L., Rajamanickam, V., & Herwig, C. (2018). The filamentous fungal pellet-relationship between morphology and productivity. Applied Microbiology and Biotechnology, 102(7), 2997-3006.
Ward, O. P. (2012). Production of recombinant proteins by filamentous fungi. Biotechnology Advances, 30(5), 1119-1139. https://doi.org/10.1016/j.biotechadv.2011.09.012
Wilde, F., Ogurreck, M., Greving, I., Hammel, J. U., Beckmann, F., Hipp, A., & Schreyer, A. (2016). Micro-CT at the imaging beamline P05 at PETRA III 030035, In AIP Conference Proceedings 1741 (p. 30035). https://doi.org/10.1063/1.4952858
Willemse, J., Büke, F., van Dissel, D., Grevink, S., Claessen, D., & van Wezel, G. P. (2018). Sparticle, an algorithm for the analysis of filamentous microorganisms in submerged cultures. Antonie Van Leeuwenhoek, 111(2), 171-182. https://doi.org/10.1007/s10482-017-0939-y
Wittier, R., Baumgartl, H., Lübbers, D. W., & Schügerl, K. (1986). Investigations of oxygen transfer into Penicillium chrysogenum pellets by microprobe measurements. Biotechnology and Bioengineering, 28(7), 1024-1036. https://doi.org/10.1002/bit.260280713
Wongwicharn, A., McNeil, B., & Harvey, L. M. (1999). Effect of oxygen enrichment on morphology, growth, and heterologous protein production in chemostat cultures of Aspergillus niger B1-D. Biotechnology and Bioengineering, 65(4), 416-424.
Wösten, H. A. B. (2019). Filamentous fungi for the production of enzymes, chemicals and materials. Current Opinion in Biotechnology, 59, 65-70. https://doi.org/10.1016/j.copbio.2019.02.010
Wucherpfennig, T., Kiep, K. A., Driouch, H., Wittmann, C., & Krull, R. (2010). Morphology and rheology in filamentous cultivations. Advances in Applied Microbiology, 72, 89-136. https://doi.org/10.1016/S0065-2164(10)72004-9
Zhang, J., & Zhang, J. (2016). The filamentous fungal pellet and forces driving its formation. Critical Reviews in Biotechnology, 36(6), 1066-1077.