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 inJournal of Water and Environment Technology Vol. 21; no. 1; pp. 49 - 58
Main Authors Ishizawa, Hidehiro, Kaji, Yukiko, Shimizu, Yuki, Kuroda, Masashi, Inoue, Daisuke, Makino, Ayaka, Nakai, Ryosuke, Tamaki, Hideyuki, Morikawa, Masaaki, Ike, Michihiko
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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.
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
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  fullname: Kuroda, Masashi
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  fullname: Inoue, Daisuke
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  organization: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Sapporo, 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
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Snippet This study reports an intriguing observation regarding the betaproteobacterium Pelomonas saccharophila MRB3 (NITE P-01647), a candidate plant growth-promoting...
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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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