Spontaneous Cell Lysis by Pelomonas saccharophila MRB3 Provides Plant-Available Macronutrients in Hydroponic Growth Media and Accelerates Biomass Production of Duckweed
This study reports an intriguing observation regarding the betaproteobacterium Pelomonas saccharophila MRB3 (NITE P-01647), a candidate plant growth-promoting bacterium that accelerates biomass production of the aquatic plant, duckweed. In a series of experiments in which strain MRB3 cells were inoc...
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Published in | Journal of Water and Environment Technology Vol. 21; no. 1; pp. 49 - 58 |
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2023
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Abstract | This study reports an intriguing observation regarding the betaproteobacterium Pelomonas saccharophila MRB3 (NITE P-01647), a candidate plant growth-promoting bacterium that accelerates biomass production of the aquatic plant, duckweed. In a series of experiments in which strain MRB3 cells were inoculated into duckweed cultures, MRB3 improved duckweed growth with decreasing cell density in the culture medium. By monitoring nutrient dynamics of plants and bacteria, we found that MRB3 exhibited spontaneous cell lysis and released NH4+ and PO43–, which were subsequently utilized for duckweed growth. Surprisingly, the amount of NH4+ released by MRB3 corresponded to approximately half of the total nitrogen contained in the inoculated cells, notwithstanding the fact that the majority of nitrogen elements in bacterial cells should be present in plant-unavailable forms, such as proteins and nucleic acids. Spontaneous cell lysis, provision of macronutrients, and duckweed growth promotion by MRB3 were robustly observed in different inoculation amounts and growth media, including natural pond water. These observations indicated the possibility of utilizing autolytic bacteria as an alternative nutrient source in hydroponic cultivation of duckweeds and other plants. |
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AbstractList | This study reports an intriguing observation regarding the betaproteobacterium Pelomonas saccharophila MRB3 (NITE P-01647), a candidate plant growth-promoting bacterium that accelerates biomass production of the aquatic plant, duckweed. In a series of experiments in which strain MRB3 cells were inoculated into duckweed cultures, MRB3 improved duckweed growth with decreasing cell density in the culture medium. By monitoring nutrient dynamics of plants and bacteria, we found that MRB3 exhibited spontaneous cell lysis and released NH4+ and PO43–, which were subsequently utilized for duckweed growth. Surprisingly, the amount of NH4+ released by MRB3 corresponded to approximately half of the total nitrogen contained in the inoculated cells, notwithstanding the fact that the majority of nitrogen elements in bacterial cells should be present in plant-unavailable forms, such as proteins and nucleic acids. Spontaneous cell lysis, provision of macronutrients, and duckweed growth promotion by MRB3 were robustly observed in different inoculation amounts and growth media, including natural pond water. These observations indicated the possibility of utilizing autolytic bacteria as an alternative nutrient source in hydroponic cultivation of duckweeds and other plants. |
ArticleNumber | 22-054 |
Author | Ishizawa, Hidehiro Tamaki, Hideyuki Nakai, Ryosuke Kuroda, Masashi Ike, Michihiko Makino, Ayaka Morikawa, Masaaki Shimizu, Yuki Kaji, Yukiko Inoue, Daisuke |
Author_xml | – sequence: 1 fullname: Ishizawa, Hidehiro organization: Graduate School of Engineering, Osaka University, Suita, Japan – sequence: 2 fullname: Kaji, Yukiko organization: Graduate School of Engineering, Osaka University, Suita, Japan – sequence: 3 fullname: Shimizu, Yuki organization: Graduate School of Engineering, Osaka University, Suita, Japan – sequence: 4 fullname: Kuroda, Masashi organization: Graduate School of Engineering, Osaka University, Suita, Japan – sequence: 5 fullname: Inoue, Daisuke organization: Graduate School of Engineering, Osaka University, Suita, Japan – sequence: 6 fullname: Makino, Ayaka organization: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Sapporo, Japan – sequence: 7 fullname: Nakai, Ryosuke organization: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Sapporo, Japan – sequence: 8 fullname: Tamaki, Hideyuki organization: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, Japan – sequence: 9 fullname: Morikawa, Masaaki organization: Graduate School of Environmental Science, Hokkaido University, Sapporo, Japan – sequence: 10 fullname: Ike, Michihiko organization: Graduate School of Engineering, Osaka University, Suita, Japan |
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Cites_doi | 10.1016/j.bcab.2019.101146 10.1007/s10725-018-0428-y 10.1038/s41467-020-18354-3 10.1111/1365-2745.13710 10.1080/00380768.2011.554223 10.6064/2012/963401 10.1038/s41598-022-04873-0 10.1016/j.idairyj.2004.08.024 10.1186/s13068-017-0746-8 10.1016/j.chemosphere.2020.129247 10.1046/j.1469-8137.2002.00463.x 10.3389/fchem.2018.00483 10.1093/femsec/fiaa101 10.1094/MPMI-06-21-0157-R 10.2166/wst.2017.296 10.1016/j.chemosphere.2019.124682 10.1016/j.wasman.2016.06.027 10.1007/s10499-021-00736-z 10.1021/es1007017 10.1016/j.jbiosc.2013.12.007 10.3390/microorganisms9061133 10.1016/0022-2836(69)90288-5 10.1128/MMBR.64.3.503-514.2000 10.1002/app.37555 10.3390/microorganisms10081564 10.1099/ijs.0.63733-0 |
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References | [1] Pan Y, Cieraad E, Armstrong J, Armstrong W, Clarkson BR, Colmer TD, Pedersen O, Visser EJW, Voesenek LACJ, van Bodegom PM: Global patterns of the leaf economics spectrum in wetlands. Nat. Commun., 11 (1), 4519, 2020. PMID:32908150, https://doi.org/10.1038/s41467-020-18354-3 [16] Xie CH, Yokota A: Reclassification of Alcaligenes latus strains IAM 12599T and IAM 12664 and Pseudomonas saccharophila as Azohydromonas lata gen. nov., comb. nov., Azohydromonas australica sp. nov. and Pelomonas saccharophila gen. nov., comb. nov., respectively. Int. J. Syst. Evol. Microbiol., 55 (6), 2419–2425, 2005. PMID:16280506, https://doi.org/10.1099/ijs.0.63733-0 [17] Suzuki W, Sugawara M, Miwa K, Morikawa M: Plant growth-promoting bacterium Acinetobacter calcoaceticus P23 increases the chlorophyll content of the monocot Lemna minor (duckweed) and the dicot Lactuca sativa (lettuce). J. Biosci. Bioeng., 118 (1), 41–44, 2014. PMID:24468072, https://doi.org/10.1016/j.jbiosc.2013.12.007 [15] Makino A, Nakai R, Yoneda Y, Toyama T, Tanaka Y, Meng XY, Mori K, Ike M, Morikawa M, Kamagata Y, Tamaki H: Isolation of aquatic plant growth-promoting bacteria for the floating plant duckweed (Lemna minor). Microorganisms, 10 (8), 1564, 2022. PMID:36013982, https://doi.org/10.3390/microorganisms10081564 [24] Lortal S, Chapot-Chartier MP: Role, mechanisms and control of lactic acid bacteria lysis in cheese. Int. Dairy J., 15 (6–9), 857–871, 2005. https://doi.org/10.1016/j.idairyj.2004.08.024 [7] Ishizawa H, Kuroda M, Morikawa M, Ike M: Evaluation of environmental bacterial communities as a factor affecting the growth of duckweed Lemna minor. Biotechnol. Biofuels, 10 (1), 62, 2017. PMID:28293292, https://doi.org/10.1186/s13068-017-0746-8 [10] Toyama T, Kuroda M, Ogata Y, Hachiya Y, Quach A, Tokura K, Tanaka Y, Mori K, Morikawa M, Ike M: Enhanced biomass production of duckweeds by inoculating a plant growth-promoting bacterium, Acinetobacter calcoaceticus P23, in sterile medium and non-sterile environmental waters. Water Sci. Technol., 76 (6), 1418–1428, 2017. PMID:28953468, https://doi.org/10.2166/wst.2017.296 [4] Appenroth KJ, Sree KS, Bog M, Ecker J, Seeliger C, Böhm V, Lorkowski S, Sommer K, Vetter W, Tolzin-Banasch K, Kirmse R, Leiterer M, Dawczynski C, Liebisch G, Jahreis G: Nutritional value of the duckweed species of the genus Wolffia (Lemnaceae) as human food. Front Chem., 6, 483, 2018. PMID:30420949, https://doi.org/10.3389/fchem.2018.00483 [27] Meeboon J, Nishida R, Iwai T, Fujiwara K, Takano M, Shinohara M: Development of soil-less substrates capable of degrading organic nitrogen into nitrate as in natural soils. Sci. Rep., 12 (1), 785, 2022. PMID:35039579, https://doi.org/10.1038/s41598-022-04873-0 [2] Ishizawa H, Onoda Y, Kitajima K, Kuroda M, Inoue D, Ike M: Coordination of leaf economics traits within the family of the world’s fastest growing plants (Lemnaceae). J. Ecol., 109 (8), 2950–2962, 2021. https://doi.org/10.1111/1365-2745.13710 [19] Japanese Industrial Standards Committee: Japanese Industrial Standard Testing Methods for Industrial Wastewater, JIS K0102. Japanese Standards Association, Tokyo, Japan, 2013. [13] Ishizawa H, Tada M, Kuroda M, Inoue D, Ike M: Performance of plant growth-promoting bacterium of duckweed under different kinds of abiotic stress factors. Biocatal. Agric. Biotechnol., 19, 101146, 2019. https://doi.org/10.1016/j.bcab.2019.101146 [8] Yamakawa Y, Jog R, Morikawa M: Effects of co-inoculation of two different plant growth-promoting bacteria on duckweed. Plant Growth Regul., 86 (2), 287–296, 2018. https://doi.org/10.1007/s10725-018-0428-y [12] Khairina Y, Jog R, Boonmak C, Toyama T, Oyama T, Morikawa M: Indigenous bacteria, an excellent reservoir of functional plant growth promoters for enhancing duckweed biomass yield on site. Chemosphere, 268, 129247, 2021. PMID:33383277, https://doi.org/10.1016/j.chemosphere.2020.129247 [11] Ishizawa H, Ogata Y, Hachiya Y, Tokura K, Kuroda M, Inoue D, Toyama T, Tanaka Y, Mori K, Morikawa M, Ike M: Enhanced biomass production and nutrient removal capacity of duckweed via two-step cultivation process with a plant growth-promoting bacterium, Acinetobacter calcoaceticus P23. Chemosphere, 238, 124682, 2020. PMID:31524619, https://doi.org/10.1016/j.chemosphere.2019.124682 [26] Stoknes K, Scholwin F, Krzesiński W, Wojciechowska E, Jasińska A: Efficiency of a novel “Food to waste to food” system including anaerobic digestion of food waste and cultivation of vegetables on digestate in a bubble-insulated greenhouse. Waste Manag., 56, 466–476, 2016. PMID:27425859, https://doi.org/10.1016/j.wasman.2016.06.027 [25] Shinohara M, Aoyama C, Fujiwara K, Watanabe A, Ohmori H, Uehara Y, Takano M: Microbial mineralization of organic nitrogen into nitrate to allow the use of organic fertilizer in hydroponics. Soil Sci. Plant Nutr., 57 (2), 190–203, 2011. https://doi.org/10.1080/00380768.2011.554223 [5] Paolacci S, Stejskal V, Jansen MAK: Estimation of the potential of Lemna minor for effluent remediation in integrated multi-trophic aquaculture using newly developed synthetic aquaculture wastewater. Aquacult. Int., 29 (5), 2101–2118, 2021. https://doi.org/10.1007/s10499-021-00736-z [9] Yoneda Y, Yamamoto K, Makino A, Tanaka Y, Meng XY, Hashimoto J, Shin-ya K, Satoh N, Fujie M, Toyama T, Mori K, Ike M, Morikawa M, Kamagata Y, Tamaki H: Novel plant-associated Acidobacteria promotes growth of common floating aquatic plants, duckweeds. Microorganisms, 9 (6), 1133, 2021. PMID:34074043, https://doi.org/10.3390/microorganisms9061133 [14] Ishizawa H, Kuroda M, Inoue D, Morikawa M, Ike M: Community dynamics of duckweed-associated bacteria upon inoculation of plant growth-promoting bacteria. FEMS Microbiol. Ecol., 96 (7), fiaa101, 2020. PMID:32445473, https://doi.org/10.1093/femsec/fiaa101 [3] Zeller MA, Hunt R, Sharma S: Sustainable bioderived polymeric materials and thermoplastic blends made from floating aquatic macrophytes such as “duckweed”. J. Appl. Polym. Sci., 127 (1), 375–386, 2013. https://doi.org/10.1002/app.37555 [18] Boyer HW, Roulland-dussoix D: A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol., 41 (3), 459–472, 1969. PMID:4896022, https://doi.org/10.1016/0022-2836(69)90288-5 [6] Yamaga F, Washio K, Morikawa M: Sustainable biodegradation of phenol by Acinetobacter calcoaceticus P23 isolated from the rhizosphere of duckweed Lemna aoukikusa. Environ. Sci. Technol., 44 (16), 6470–6474, 2010. PMID:20704249, https://doi.org/10.1021/es1007017 [23] Lewis K: Programmed death in bacteria. Microbiol. Mol. Biol. Rev., 64 (3), 503–514, 2000. PMID:10974124, https://doi.org/10.1128/MMBR.64.3.503-514.2000 [22] Glick BR: Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo), 2012, 1–15, 2012. PMID:24278762, https://doi.org/10.6064/2012/963401 [20] Cedergreen N, Madsen TV: Nitrogen uptake by the floating macrophyte Lemna minor. New Phytol., 155 (2), 285–292, 2002. https://doi.org/10.1046/j.1469-8137.2002.00463.x [21] Toyama T, Mori K, Tanaka Y, Ike M, Morikawa M: Growth promotion of giant duckweed Spirodela polyrhiza (Lemnaceae) by Ensifer sp. SP4 through enhancement of nitrogen metabolism and photosynthesis. Mol. Plant Microbe Interact., 35 (1), 28–38, 2022. PMID:34622686, https://doi.org/10.1094/MPMI-06-21-0157-R 22 23 24 25 26 27 10 11 12 13 14 15 16 17 18 19 1 2 3 4 5 6 7 8 9 20 21 |
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SubjectTerms | Aquatic plants Bacteria bacterial autolysis Biomass Cell culture Cell density Cells Culture media Duckweed Floating plants Freshwater plants Growth media Hydroponics Inoculation Lysis Nitrogen Nucleic acids Nutrient dynamics Plant growth plant growth-promoting bacteria Plants |
Title | Spontaneous Cell Lysis by Pelomonas saccharophila MRB3 Provides Plant-Available Macronutrients in Hydroponic Growth Media and Accelerates Biomass Production of Duckweed |
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