Instrumental use of Marine Bacteria to Stimulate Growth in Seaweed

Year 2024, Volume: 30 Issue: 3, 501 - 512, 23.07.2024

Pham Thi Mien Phan Minh-thu Bui Thi Ngoc Trieu Nguyen Minh Hieu Dao Viet Ha

https://doi.org/10.15832/ankutbd.1386116

Abstract

Edible seaweed - Caulerpa lentillifera is being cultivated along the coast of Khanh Hoa province, Vietnam, and makes a relatively large contribution to the economic development of this region. Bacterial strains originating from marine sources such as those associated with seaweed and hard coral were screened for properties of promote plant growth with the capacity of indole-3-acetic acid (IAA) - a phytohormone belonging to auxin group, the phosphate solubilization ability and antibacterial activity of IAA-producing strains were also performed in this study. Robust strains were identified by morphological methods with biochemical tests and analysis of 16s RNA sequences. Isolate RN06 produced high amounts of IAA, utilized inorganic phosphate, and inhibited Bacillus subtilis ATCC6633, Escherichia coli 0157, and Serratia marcescens PDL100. The IAA producer HRA5 isolated from hard coral demonstrated the ability to solubilize phosphate and exhibited antibacterial activity against B. subtilis. Morphological analysis and 16sRNA sequencing showed that isolate RN06 was the closest strain to Bacillus amyloliquefaciens and HRA5 was linked to Pseudomonas sp. This is the first report of isolated bacteria from seaweed and corals from the Vietnamese sea served as potential strains for further research of the application of biological inoculants specifically for seaweed farming.

Keywords

indole-3-acetic acid-producing bacteria, phosphate solubilizing bacteria, antimicrobial activity, marine potential bacteria

Ethical Statement

N/A

Supporting Institution

VAST key lab for food and environment safety in the center of Vietnam, Institute of Oceanography - VAST for providing facilities to conduct this experiment

Project Number

The project of the Vietnam Academy of Science and Technology, grant number CSCL17.02/23-24

Thanks

Mr Phan Kim Hoang for sampling and identification of corals

References

• Ahmad B, Nigar S, Malik N A, Bashir S, Ali J, Yousaf S, Bangash J A & Jan I (2013). Isolation and Characterization of Cellulolytic Nitrogen Fixing Azotobacter species from Wheat Rhizosphere of Khyber Pakhtunkhwa. World Applied Sciences Journal 27 (1): 51-60. 10.5829/idosi.wasj.2013.27.01.81120
• Ali B, Sabri A N, Ljung K & Hasnain S (2009). Auxin production by plant associated bacteria: impact on endogenous IAA content and growth of Triticum aestivum L. Lett Appl Microbiol 48(5): 542-547. https://doi.org/10.1111/j.1472-765X.2009.02565.x
• Amin S A, Hmelo L R, van Tol H M, Durham B P, Carlson L T, Heal K R, Morales R L, Berthiaume C T, Parker M S, Djunaedi B, Ingalls A E, Parsek M R, Moran M A & Armbrust E V (2015). Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522: 98-101. https://doi.org/10.1038/nature14488
• Bauer A W, Kirby W M, Sherris J C & Turck M (1966). Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathogens 45: 493-496,
• Bharucha U, Patel K & Trivedi U B (2013). Optimization of Indole Acetic Acid Production by Pseudomonas putida UB1 and its Effect as Plant Growth-Promoting Rhizobacteria on Mustard (Brassica nigra). Agricultural Research 2(3): 215-221. https://doi.org/10.1007/s40003-013-0065-7
• Bogaert K A, Blommaert L, Ljung K, Beeckman T & De Clerck O (2019). Auxin Function in the Brown Alga Dictyota dichotoma. Plant Physiol 179(1): 280-299. https://doi.org/10.1104/pp.18.01041
• Buller N B (2014). Bacteria and Fungi from Fish and Other Aquatic Animals. ISBN-13: 978 1 84593 805 5 ed. Centre for Agriculture and Bioscience International (CABI), Oxfordshire, UK,
• Chen X, Sun Y, Liu H, Liu S, Qin Y & Li P (2019). Advances in cultivation, wastewater treatment application, bioactive components of Caulerpa lentillifera and their biotechnological applications. PeerJ 7: e6118-e6118. https://doi.org/10.7717/peerj.6118
• Comeau D, Balthazar C, Novinscak A, Bouhamdani N, Joly D L & Filion M (2021). Interactions Between Bacillus Spp., Pseudomonas Spp. and Cannabis sativa Promote Plant Growth. Frontiers in Microbiology 12. https://doi.org/10.3389/fmicb.2021.715758
• Cooper R (1959). Bacterial fertilizers in the Soviet Union. Soils Fertil. 22: 327–333,
• de Castro A P, Araujo S D J, Reis A M, Moura R L, Francini-Filho R B, Pappas G, Jr, Rodrigues T B, Thompson F L & Kruger R H (2010). Bacterial community associated with healthy and diseased reef coral Mussismilia hispida from eastern Brazil. Microb. Ecol 59: 658-667. https://doi.org/10.1007/s00248-010-9646-1
• de Oliveira Mendes G, Moreira de Freitas A L, Liparini Pereira O, Ribeiro da Silva I, Bojkov Vassilev N & Dutra Costa M (2014). Mechanisms of phosphate solubilization by fungal isolates when exposed to different P sources. Annals of Microbiology 64(1): 239-249. https://doi.org/10.1007/s13213-013-0656-3
• del Olmo A, Picon A & Nuñez M (2018). The microbiota of eight species of dehydrated edible seaweeds from North West Spain. Food Microbiology 70: 224-231. https://doi.org/10.1016/j.fm.2017.10.009
• Dittami S M, Barbeyron T, Boyen C, Cambefort J, Collet G, Delage L, Gobet A, Groisillier A, Leblanc C, Michel G, Scornet D, Siegel A, Tapia J E & Tonon T (2014). Genome and metabolic network of “Candidatus Phaeomarinobacter ectocarpi” Ec32, a new candidate genus of Alphaproteobacteria frequently associated with brown algae. Frontiers in Genetics 5: 241-254. https://doi.org/10.3389/fgene.2014.00241
• Gong Y, Bai J L, Yang H T, Zhang W D, Xiong Y W, Ding P & Qin S (2018). Phylogenetic diversity and investigation of plant growth-promoting traits of actinobacteria in coastal salt marsh plant rhizospheres from Jiangsu, China. Syst Appl Microbiol 41(5): 516-527. https://doi.org/10.1016/j.syapm.2018.06.003
• Gordon S A & Paleg L G (1957). Observations on the Quantitative Determination of Indoleacetic Acid. Physiol. Plant 10: 39–47
• Goswami D, Dhandhukia P, Patel P & Thakker J N (2014). Screening of PGPR from saline desert of Kutch: growth promotion in Arachis hypogea by Bacillus licheniformis A2. Microbiol Res 169(1): 66-75. https://doi.org/10.1016/j.micres.2013.07.004
• Grossmann K (2003). Mediation of Herbicide Effects by Hormone Interactions. Journal of Plant Growth Regulation 22(1): 109-122. https://doi.org/10.1007/s00344-003-0020-0
• Gupta M, Kiran S, Gulati A, Singh B & Tewari R (2012). Isolation and identification of phosphate solubilizing bacteria able to enhance the growth and aloin-A biosynthesis of Aloe barbadensis Miller. Microbiol Res 167(6): 358-363. https://doi.org/10.1016/j.micres.2012.02.004
• Gutierrez C K, Matsui G Y, Lincoln D E & Lovell C R (2009). Production of the phytohormone indole-3-acetic acid by estuarine species of the genus Vibrio. Appl Environ Microbiol 75(8): 2253-2258. https://doi.org/10.1128/AEM.02072-08
• Gyaneshwar P, Parekh L J, Archana G, Poole P S, Collins M D, Hutson R A & Kumar G N (1999). Involvement of a phosphate starvation inducible glucose dehydrogenase in soil phosphate solubilization by Enterobacter asburiae. FEMS Microbiology Letters 171(2): 223-229. https://doi.org/10. 1111/j.1574-6968.1999.tb13436.x
• Halebian S, Harris B, Finegold S M & Rolfe R D (1981). Rapid method that aids in distinguishing Gram-positive from Gram-negative anaerobic bacteria. Journal of clinical microbiology 13(3): 444-448. https://doi.org/10.1128/jcm.13.3.444-448.1981
• Ismail A, Ktari L, Ahmed M, Bolhuis H, Boudabbous A, Stal L J, Cretoiu M S & El Bour M (2016). Antimicrobial Activities of Bacteria Associated with the Brown Alga Padina pavonica. Front Microbiol 7: 1072-1085. https://doi.org/10.3389/fmicb.2016.01072
• Jeon J-S, Lee S-S, Kim H-Y, Ahn T-S & Song H-G (2003). Plant Growth Promotion in Soil by Some Inoculated Microorganisms. The Journal of Microbiology 41(4): 271-276,
• Karthick P & Mohanraju R (2018). Antimicrobial Potential of Epiphytic Bacteria Associated With Seaweeds of Little Andaman, India. Front Microbiol 9: 611. https://doi.org/10.3389/fmicb.2018.00611
• Khan A L, Halo B A, Elyassi A, Ali S, Al-Hosni K, Hussain J, Al-Harrasi A & Lee I-J (2016). Indole acetic acid and ACC deaminase from endophytic bacteria improves the growth of Solanum lycopersicum. Electronic Journal of Biotechnology 21: 58-64. https://doi.org/10.1016/j.ejbt.2016.02.001
• Le Bail A, Billoud B, Kowalczyk N, Kowalczyk M, Gicquel M, Le Panse S, Stewart S, Scornet D, Cock J M, Ljung K & Charrier B (2010). Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus. Plant physiology 153(1): 128-144. https://doi.org/10.1104/pp.109.149708
• Leyser O (2010). The power of auxin in plants. Plant Physiol 154(2): 501-505. https://doi.org/10.1104/pp.110.161323
• Lin H, Li Y & Hill R T (2022). Microalgal and bacterial auxin biosynthesis: implications for algal biotechnology. Current Opinion in Biotechnology 73: 300-307. https://doi.org/10.1016/j.copbio.2021.09.006
• Logan N A & Berkeley R C (1984). Identification of Bacillus Strains Using the API System. Journal of General Microbiology 130(7): 1871-1882
• Maruyama A, Maeda M & Simidu U (1989). Microbial production of auxin indole-3-acetic acid in marine sediments. Marine Ecology Progress Series 58(1/2): 69-75. http://www.jstor.org/stable/24842169
• Mayers T J, Bramucci A R, Yakimovich K M & Case R J (2016). A Bacterial Pathogen Displaying Temperature-Enhanced Virulence of the Microalga Emiliania huxleyi. Frontiers in Microbiology 7. 10.3389/fmicb.2016.00892
• Mishra A K & Kefford N P (1969). Developmental studies on the coenocytic alga, Caulerpa sertularioides. J Phycol 5(2): 103-109. https://doi.org/10.1111/j.1529-8817.1969.tb02586.x
• Nguyen K H, Pham T M, Bui H H & Vo H T (2016). Screening of coral associated bacteria with antimicrobial activities from scleractinian coral Acropora muricata in the Nha Trang bay. The Collection of Marine Work (in Vietnamese) 22: 83-95
• Palomo S, González I, de la Cruz M, Martín J, Tormo J R, Anderson M, Hill R T, Vicente F, Reyes F & Genilloud O (2013). Sponge-derived Kocuria and Micrococcus spp. as sources of the new thiazolyl peptide antibiotic kocurin. Marine drugs 11(4): 1071-1086. https://doi.org/10.3390/md11041071
• Park J-M, Radhakrishnan R, Kang S-M & Lee I-J (2015). IAA Producing Enterobacter sp. I-3 as a Potent Bio-herbicide Candidate for Weed Control: A Special Reference with Lettuce Growth Inhibition. Indian journal of microbiology 55(2): 207-212. https://doi.org/10.1007/s12088-015-0515-y
• Paul D & Sinha S N (2017). Isolation and characterization of phosphate solubilizing bacterium Pseudomonas aeruginosa KUPSB12 with antibacterial potential from river Ganga, India. Annals of Agrarian Science 15(1): 130-136. https://doi.org/10.1016/j.aasci.2016.10.001
• Pham T M (2014). Community of soft coral Alcyonium digitatum associated bacteria and their antimicrobial activities. PhD Thesis, Christian-Albrecht University of Kiel, GEOMAR in Kiel, Germany.
• Pham T M, Nguyen K H, Nguyen M H, Phan M T, Hoang T D, Vo H T, Nguyen T D H, Le T D & Nguyen H H (2019). A study on bacteria associated with three hard coral species from Ninh Thuan by epifluorescence and most diluted culture method. Vietnam Journal of Marine Science and Technology 19(2): 271-283. https://doi.org/10.15625/1859-3097/19/2/10814
• Pham T M, Nguyen N T & Nguyen K H (2018). Bacillus sp. VK2 isolated from Acropora hyacinthus from Ninh Thuan and its antimicrobial activities against cause of white pox disease in Acropora palmate. Vietnam Journal of Marine Science and Technology 18(2): 197-204. https://doi.org/10.15625/1859-3097/18/2/8766
• Rawat P, Das S, Shankhdhar D & Shankhdhar S C (2021). Phosphate-Solubilizing Microorganisms: Mechanism and Their Role in Phosphate Solubilization and Uptake. Journal of Soil Science and Plant Nutrition 21(1): 49-68. https://doi.org/10.1007/s42729-020-00342-7
• Sánchez-Cruz R, Tpia Vázquez I, Batista-García R A, Méndez-Santiago E W, Sánchez-Carbente M d R, Leija A, Lira-Ruan V, Hernández G, Wong-Villarreal A & Folch-Mallol J L (2019). Isolation and characterization of endophytes from nodules of Mimosa pudica with biotechnological potential. Microbiological Research 218: 76-86. https://doi.org/10.1016/j.micres.2018.09.008
• Sunarpi H, Nikmatullah A, Ambana Y, Ilhami B T K, Abidin A S, Ardiana N, Kirana I A P, Kurniawan N S H, Rinaldi R, Jihadi A & Prasedya E S (2021). Phytohormone content in brown macroalgae Sargassum from Lombok coast, Indonesia. IOP Conference Series: Earth and Environmental Science 712(1): 012042. https://doi.org/10.1088/1755-1315/712/1/012042
• Tao C, Yuan C, Ruan C, Chen Q & Lin W (2017). Effects of different phytohormones on the growth of Caulerpa lentillifera. . Journal of Fuzhou University (Natural Science Edition) 45(2): 291–295
• Tirtawijaya G, Negara B F S P, Lee J-H, Cho M-G, Kim H K, Choi Y-S, Lee S-H & Choi J-S (2022). The Influence of Abiotic Factors on the Induction of Seaweed Callus. Journal of Marine Science and Engineering 10(4): 513. https://doi.org/10.3390/jmse10040513
• Vasanthabharathi V & Jayalakshmi S (2017). Diversity and Distribution of Indole Acetic Acid Producing Marine Sponge Associated Bacteria from Gulf of Mannar, Southeast Coast of India. Global Veterinaria 19(1): 487-490. https://doi.org/10.5829/idosi.gv.2017.487.490
• Yazdani M, Bahmanyar M A, Pirdashti H & A E M (2009). Effect of phosphate solubilization microorganisms (PSM) and plant growth promoting rhizobacteria (PGPR) on yield and yield components of corn (Zea mays L.). Proc. World Acad. Science 37: 90-92. https://doi.org/10.5281/zenodo.1080014
• Zhang X, Sun Y, Bao J, He F, Xu X & Qi S (2012). Phylogenetic survey and antimicrobial activity of culturable microorganisms associated with the South China Sea black coral Antipathes dichotoma. FEMS Microbiol. Lett 336: 122-130. https://doi.org/10.1111/j.1574-6968.2012.02662.x