Effects of ferric ions on the capacity of Shewanella marisflavi ECSMB14101 biofilms to induce the settlement and metamorphosis of Mytilus coruscus
Author:
Clc Number:

S968.3

  • Article
  • | |
  • Metrics
  • |
  • Reference [48]
  • |
  • Related [20]
  • | | |
  • Comments
    Abstract:

    To study the impact of ferric ions on the ability of Shewanella marisflavi ECSMB14101 biofilms to induce larval settlement and metamorphosis in Mytilus coruscus, single bacterial biofilms cultivated with different ferric ion concentrations were used to induce larval settlement and metamorphosis. The effects of ferric ion concentration on the inducing activity of larval settlement and metamorphosis, bacterial density, extracellular polymeric substances, and cytochrome C content of S. marisflavi biofilms were analysed. Results showed that among the seven groups with ferric ion concentrations of 0, 1, 10, 20, 30, 40, and 50 μmol/L, the biofilm of S. marisflavi cultivated at a concentration of 20 μmol/L exhibited the highest inducing activity. Furthermore, at this concentration, both the bacterial density of the biofilm and the levels of extracellular proteins and cytochrome C reached their peak among all seven tested concentrations. Extracellular polysaccharides and lipids were not significantly affected by ferric ion concentration. It was shown that under the effects of ferric ions, S. marisflavi biofilms regulate the larval settlement and metamorphosis in M. coruscus by modulating the production of extracellular proteins, including cytochrome C. This research offered a solid theoretical foundation and served as a valuable reference for the in-depth investigation of the molecular regulatory mechanisms underlying larval settlement and metamorphosis in M. coruscus. Additionally, it contributes to the understanding of interactions between shellfish and bacteria.

    Reference
    [1] QIAN P Y, CHENG A F, WANG R J, et al. Marine biofilms: diversity, interactions and biofouling[J]. Nature Reviews Microbiology, 2022, 20(11): 671-684.
    [2] STRATHMANN R R. Hypotheses on the origins of marine larvae[J]. Annual Review of Ecology, Evolution, and Systematics, 1993, 24(1): 89-117.
    [3] HADFIELD M G, CARPIZO-ITUARTE E J, DEL CARMEN K, et al. Metamorphic competence, a major adaptive convergence in marine invertebrate larvae[J]. American Zoologist, 2001, 41(5): 1123-1131.
    [4] ALMEDA R, RIST S, CHRISTENSEN A M, et al. Crude oil and its burnt residues induce metamorphosis in marine invertebrates[J]. Environmental Science & Technology, 2023, 57(48): 19304-19315.
    [5] CARBONNE C, COMEAU S, CHAN P T W, et al. Early life stages of a Mediterranean coral are vulnerable to ocean warming and acidification[J]. Biogeosciences, 2022, 19(19): 4767-4777.
    [6] SIDDIK A A, SATHEESH S. Interactive effects of light and substrate colour on the recruitment of marine invertebrates on artificial materials[J]. Community Ecology, 2021, 22(1): 69-78.
    [7] WANG C, BAO W Y, GU Z Q, et al. Larval settlement and metamorphosis of the mussel Mytilus coruscus in response to natural biofilms[J]. Biofouling, 2012, 28(3): 249-256.
    [8] HARDER T, QIAN P Y. Induction of larval attachment and metamorphosis in the serpulid polychaete Hydroides elegans by dissolved free amino acids: isolation and identification[J]. Marine Ecology Progress Series, 1999, 179: 259-271.
    [9] SHEN S Y, SUN X H, XU Y N, et al. Effects of ultra-high pressure (UHP) processing on biofilm formation of Listeria monocytogenes[J]. Journal of Shanghai Ocean University, 2017, 26(2): 294-300. 莘似韵, 孙晓红, 徐忆宁, 等. 超高压对单增李斯特菌生物被膜形成的影响[J]. 上海海洋大学学报, 2017, 26(2): 294-300.
    [10] FU J J, WANG X, LIU H Q, et al. Effects of sigB on biofilm formation by Listeria monocytogenes under various culture conditions[J]. Journal of Shanghai Ocean University, 2016, 25(4): 634-640. 付娇娇, 王旭, 刘海泉, 等. 不同培养条件下sigB对单增李斯特菌生物被膜形成的影响[J]. 上海海洋大学学报, 2016, 25(4): 634-640.
    [11] YANG N, RØDER H L, WICAKSONO W A, et al. Interspecific interactions facilitate keystone species in a multispecies biofilm that promotes plant growth[J]. The ISME Journal, 2024, 18(1): wrae012.
    [12] SHI H J, MAO X S, YANG F, et al. Multi-scale analysis of acidophilic microbial consortium biofilm's tolerance of lithium and cobalt ions in bioleaching[J]. Journal of Hazardous Materials, 2024, 474: 134764.
    [13] BANIN E, VASIL M L, PETER GREENBERG E. Iron and Pseudomonas aeruginosa biofilm formation[J]. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(31): 11076-11081.
    [14] DONG Y R, SHAN Y W, XIA K M, et al. The proposed molecular mechanisms used by archaea for Fe(III) reduction and Fe(II) oxidation[J]. Frontiers in Microbiology, 2021, 12: 690918.
    [15] MÜHLENHOFF U, BRAYMER J J, CHRIST S, et al. Glutaredoxins and iron-sulfur protein biogenesis at the interface of redox biology and iron metabolism[J]. Biological Chemistry, 2020, 401(12): 1407-1428.
    [16] RODEN E E. Microbial iron-redox cycling in subsurface environments[J]. Biochemical Society Transactions, 2012, 40(6): 1249-1256.
    [17] QIN Y X, HE Y H, SHE Q X, et al. Heterogeneity in respiratory electron transfer and adaptive iron utilization in a bacterial biofilm[J]. Nature Communications, 2019, 10(1): 3702.
    [18] CORNELIS P, MATTHIJS S, VAN OEFFELEN L. Iron uptake regulation in Pseudomonas aeruginosa[J]. BioMetals, 2009, 22(1): 15-22.
    [19] CHEN X, STEWART P S. Role of electrostatic interactions in cohesion of bacterial biofilms[J]. Applied Microbiology and Biotechnology, 2002, 59(6): 718-720.
    [20] WIENS J R, VASIL A I, SCHURR M J, et al. Iron-regulated expression of alginate production, mucoid phenotype, and biofilm formation by Pseudomonas aeruginosa[J]. mBio, 2014, 5(1): e01010-13.
    [21] CHANG R H, XU K H, CAI Y S, et al. Effects of calcium on biofilm formation of the bacterium Pseudoalteromonas marina and settlement of mussel Mytilus coruscus[J]. Journal of Dalian Ocean University, 2020, 35(6): 893-900. 常睿珩, 许康豪, 蔡雨珊, 等. 钙离子对海假交替单胞菌生物被膜形成及厚壳贻贝附着的影响[J]. 大连海洋大学学报, 2020, 35(6): 893-900.
    [22] YANG J L, SHEN P J, LIANG X, et al. Larval settlement and metamorphosis of the mussel Mytilus coruscus in response to monospecific bacterial biofilms[J]. Biofouling, 2013, 29(3): 247-259.
    [23] GONZÁLEZ-MACHADO C, CAPITA R, RIESCO-PELÁEZ F, et al. Visualization and quantification of the cellular and extracellular components of Salmonella Agona biofilms at different stages of development[J]. PLoS One, 2018, 13(7): e0200011.
    [24] O'TOOLE G, KAPLAN H B, KOLTER R. Biofilm formation as microbial development[J]. Annual Review of Microbiology, 2000, 54(1): 49-79.
    [25] BRANDA S S, VIK Å, FRIEDMAN L, et al. Biofilms: the matrix revisited[J]. Trends in Microbiology, 2005, 13(1): 20-26.
    [26] LIN M H, SHU J C, HUANG H Y, et al. Involvement of iron in biofilm formation by Staphylococcus aureus[J]. PLoS One, 2012, 7(3): e34388.
    [27] OH E, ANDREWS K J, JEON B. Enhanced biofilm formation by ferrous and ferric iron through oxidative stress in Campylobacter jejuni[J]. Frontiers in Microbiology, 2018, 9: 1204.
    [28] YU S, WEI Q, ZHAO T H, et al. A survival strategy for Pseudomonas aeruginosa that uses exopolysaccharides to sequester and store iron to stimulate Psl-dependent biofilm formation[J]. Applied and Environmental Microbiology, 2016, 82(21): 6403-6413.
    [29] MUSK D J, BANKO D A, HERGENROTHER P J. Iron salts perturb biofilm formation and disrupt existing biofilms of Pseudomonas aeruginosa[J]. Chemistry & Biology, 2005, 12(7): 789-796.
    [30] CHANG W W, LI Y Y, LI Z Y, et al. The effect of riboflavin on the microbiologically influenced corrosion of pure iron by Shewanella oneidensis MR-1[J]. Bioelectrochemistry, 2022, 147: 108173.
    [31] FREDRICKSON J K, ROMINE M F, BELIAEV A S, et al. Towards environmental systems biology of Shewanella[J]. Nature Reviews Microbiology, 2008, 6(8): 592-603.
    [32] LEMAIRE O N, MÉJEAN V, IOBBI-NIVOL C. The Shewanella genus: ubiquitous organisms sustaining and preserving aquatic ecosystems[J]. FEMS Microbiology Reviews, 2020, 44(2): 155-170.
    [33] CHANG R H, FENG D D, PENG L H, et al. Complete genome sequence of Shewanella marisflavi ECSMB14101, a red pigment synthesizing bacterium isolated from the East China Sea[J]. Marine Genomics, 2021, 58: 100846.
    [34] FRANCESCA B, AJELLO M, BOSSO P, et al. Both lactoferrin and iron influence aggregation and biofilm formation in Streptococcus mutans[J]. Biometals, 2004, 17(3): 271-278.
    [35] MA L Z, WANG D, LIU Y W, et al. Regulation of biofilm exopolysaccharide biosynthesis and degradation in Pseudomonas aeruginosa[J]. Annual Review of Microbiology, 2022, 76(1): 413-433.
    [36] HADFIELD M G. Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites[J]. Annual Review of Marine Science, 2011, 3(1): 453-470.
    [37] SHIKUMA N J, PILHOFER M, WEISS G L, et al. Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures[J]. Science, 2014, 343(6170): 529-533.
    [38] LIANG X, ZHANG X K, PENG L H, et al. The flagellar gene regulates biofilm formation and mussel larval settlement and metamorphosis[J]. International Journal of Molecular Sciences, 2020, 21(3): 710.
    [39] CHEN H E, HE K, HE C H, et al. Effects of alginate on biofilm formation of Pseudoalteromonas marina and larval settlement and metamorphosis of the mussel Mytilus coruscus[J]. Journal of Dalian Fisheries University, 2022, 37(4): 620-626. 陈慧娥, 贺康, 贺楚晗, 等. 藻酸盐对海假交替单胞菌生物被膜形成及厚壳贻贝附着变态的影响[J]. 大连海洋大学学报, 2022, 37(4): 620-626.
    [40] WU J X, LI J Z, HU X M, et al. Effects of lipopolysaccharide on biofilm formation and larval metamorphosis of the mussel Mytilus coruscus[J]. Journal of Fisheries of China, 2022, 46(11): 2134-2142. 吴静娴, 李嘉政, 胡晓梦, 等. 脂多糖对细菌生物被膜形成及厚壳贻贝幼虫变态的影响[J]. 水产学报, 2022, 46(11): 2134-2142.
    [41] JIANG X J, WANG X D. Cytochrome c-mediated apoptosis[J]. Annual Review of Biochemistry, 2004, 73(1): 87-106.
    [42] HU W Y, YAO C L. Molecular and immune response characterizations of a novel AIF and cytochrome c in Litopenaeus vannamei defending against WSSV infection[J]. Fish & Shellfish Immunology, 2016, 56: 84-95.
    [43] PIRGER Z, RÁCZ B, KISS T. Dopamine-induced programmed cell death is associated with cytochrome c release and caspase-3 activation in snail salivary gland cells[J]. Biology of the Cell, 2009, 101(2): 105-116.
    [44] ROBERTSON A J, CROCE J, CARBONNEAU S, et al. The genomic underpinnings of apoptosis in Strongylocentrotus purpuratus[J]. Developmental Biology, 2006, 300(1): 321-334.
    [45] LIU Z X, LI J Z, LIANG L L, et al. Molecular cloning of McCaspase 3-4and its functions in Mytilus coruscus larval metamorphosis[J]. Acta Hydrobiologica Sinica, 2022, 46(8): 1168-1176. 刘志显, 李嘉政, 梁邻利, 等. 厚壳贻贝McCaspase 3-4基因的克隆及其在幼虫变态中的作用[J]. 水生生物学报, 2022, 46(8): 1168-1176.
    [46] WANG Y, LING N, WANG Y P, et al. Effect of ferric ions on Cronobacter sakazakii growth, biofilm formation, and swarming motility[J]. International Journal of Food Microbiology, 2024, 408: 110418.
    [47] SMITH L J, KAHRAMAN A, THORNTON J M. Heme proteins—diversity in structural characteristics, function, and folding[J]. Proteins: Structure, Function, and Bioinformatics, 2010, 78(10): 2349-2368.
    [48] WU Y, YAO J J, YANG R J, et al. Distribution and mixing behavior of dissolved iron in the Changjiang River Estuary during summer[J]. Marine Sciences, 2022, 46(11): 15-28. 吴瑶, 姚佳佳, 杨茹君, 等. 夏季长江口海域溶解态铁的分布及混合行为研究[J]. 海洋科学, 2022, 46(11): 15-28.
    Cited by
    Comments
    Comments
    分享到微博
    Submit
Get Citation

陶钰,马蕃,彭莉华,梁箫,杨金龙.铁离子对海洋希瓦氏菌生物被膜诱导厚壳贻贝附着变态能力的影响[J].上海海洋大学学报,2025,34(1):69-79.
TAO Yu, MA Fan, PENG Lihua, LIANG Xiao, YANG Jinlong. Effects of ferric ions on the capacity of Shewanella marisflavi ECSMB14101 biofilms to induce the settlement and metamorphosis of Mytilus coruscus[J]. Journal of Shanghai Ocean University,2025,34(1):69-79.

Copy
Share
Article Metrics
  • Abstract:69
  • PDF: 612
  • HTML: 48
  • Cited by: 0
History
  • Received:September 30,2024
  • Revised:December 09,2024
  • Adopted:December 26,2024
  • Online: January 22,2025
Article QR Code