Skip to main content
Log in

Antagonistic Interactions and Biofilm Forming Capabilities Among Bacterial Strains Isolated from the Egg Surfaces of Lake Sturgeon (Acipenser fulvescens)

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Characterization of interactions within a host-associated microbiome can help elucidate the mechanisms of microbial community formation on hosts and can be used to identify potential probiotics that protect hosts from pathogens. Microbes employ various modes of antagonism when interacting with other members of the community. The formation of biofilm by some strains can be a defense against antimicrobial compounds produced by other taxa. We characterized the magnitude of antagonistic interactions and biofilm formation of 25 phylogenetically diverse taxa that are representative of isolates obtained from egg surfaces of the threatened fish species lake sturgeon (Acipenser fulvescens) at two ecologically relevant temperature regimes. Eight isolates exhibited aggression to at least one other isolate. Pseudomonas sp. C22 was found to be the most aggressive strain, while Flavobacterium spp. were found to be one of the least aggressive and the most susceptible genera. Temperature affected the prevalence and intensity of antagonism. The aggressive strains identified also inhibited growth of known fish pathogens. Biofilm formations were observed for nine isolates and were dependent on temperature and growth medium. The most aggressive of the isolates disrupted biofilm formation of two well-characterized isolates but enhanced biofilm formation of a fish pathogen. Our results revealed the complex nature of interactions among members of an egg associated microbial community yet underscored the potential of specific microbial populations as host probiotics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Hungate RE, Bryant MP, Mah RA (1964) The rumen bacteria and protozoa Annu. Rev. Microbiol. 18:131–166. doi:10.1146/annurev.mi.18.100164.001023

    Article  PubMed  CAS  Google Scholar 

  2. Schultz JE, Breznak JA (1978) Heterotrophic bacteria present in hindguts of wood-eating termites Reticulitermes flavipes (Kollar) Appl. Environ. Microbiol. 35:930–936

    PubMed  PubMed Central  CAS  Google Scholar 

  3. Biswas SR, Wagner HH (2012) Landscape contrast: a solution to hidden assumptions in the metacommunity concept? Landsc. Ecol. 27:621–631. doi:10.1007/s10980-012-9732-5

    Article  Google Scholar 

  4. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A (2004) The metacommunity concept: a framework for multi-scale community ecology Ecol. Lett. 7:601–613. doi:10.1111/j.1461-0248.2004.00608.x

    Article  Google Scholar 

  5. Biagi E, Candela M, Fairweather-Tait S, Franceschi C, Brigidi P (2012) Ageing of the human metaorganism: the microbial counterpart Age 34:247–267. doi:10.1007/s11357-011-9217-5

    Article  PubMed  Google Scholar 

  6. Bosch TCG, McFall-Ngai MJ (2011) Metaorganisms as the new frontier Zoology 114:185–190. doi:10.1016/j.zool.2011.04.001

    Article  PubMed  Google Scholar 

  7. Barnes ME, Bergmann D, Stephenson H, Gabel M, Cordes RJ (2005) Bacterial numbers from landlocked fall Chinook salmon eyed eggs subjected to various formalin treatments as determined by scanning electron microscopy and bacteriological culture methods N. Am. J. Aquac. 67:23–33

    Article  Google Scholar 

  8. Hansen GH, Olafsen JA (1989) Bacterial-colonization of cod (Gadus-Morhua L) and halibut (Hippoglossus-Hippoglossus) eggs in marine aquaculture Appl. Environ. Microbiol. 55:1435–1446

    PubMed  PubMed Central  CAS  Google Scholar 

  9. Hansen GH, Olafsen JA (1999) Bacterial interactions in early life stages of marine cold water fish Microb. Ecol. 38:1–26

    Article  PubMed  CAS  Google Scholar 

  10. Hibbing ME, Fuqua C, Parsek MR, Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle Nat Rev Microbiol 8:15–25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Hoffman LR, D'Argenio DA, MacCoss MJ, Zhang Z, Jones RA, Miller SI (2005) Aminoglycoside antibiotics induce bacterial biofilm formation Nature 436:1171–1175 http://www.nature.com/nature/journal/v436/n7054/suppinfo/nature03912_S1.html

    Article  PubMed  CAS  Google Scholar 

  12. Narisawa N, Haruta S, Arai H, Ishii M, Igarashi Y (2008) Coexistence of Antibiotic-producing and Antibiotic-sensitive bacteria in biofilms is mediated by resistant bacteria Appl. Environ. Microbiol. 74:3887–3894. doi:10.1128/aem.02497-07

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Burmølle M, Webb JS, Rao D, Hansen LH, Sørensen SJ, Kjelleberg S (2006) Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms Appl. Environ. Microbiol. 72:3916–3923. doi:10.1128/aem.03022-05

    Article  PubMed  PubMed Central  Google Scholar 

  14. Anderson GG, Palermo JJ, Schilling JD, Roth R, Heuser J, Hultgren SJ (2003) Intracellular bacterial biofilm-like pods in urinary tract infections Science 301:105–107. doi:10.1126/science.1084550

    Article  PubMed  CAS  Google Scholar 

  15. Baker EA, Borgeson DJ (1999) Lake sturgeon abundance and harvest in black Lake, Michigan, 1975-1999 N Am J Fish Manag 19:1080–1088

    Article  Google Scholar 

  16. Smith KM, Baker EA (2005) Characteristics of spawning lake sturgeon in the upper Black River, Michigan N Am J Fish Manag 25:301–307. doi:10.1577/m03-229.1

    Article  Google Scholar 

  17. Forsythe PS (2010) Exogenous correlates of migration, spawning, egg deposition and egg mortality in the lake sturgeon (Acipenser fulvescens). Ph.D. Dissertation. Department of Fisheries and Wildlife. Michigan State University. #3417681. pp191

  18. Fujimoto M (2012) Microbial succession on the lake sturgeon egg surface: Mechanisms shaping the microbial community assembly during succession and the effect of microbial successional processes on host life history traits. Ph.D. Dissertation, Department of Microbiology and Molecular Genetics, Michigan State University. #3548462. pp201

  19. Fujimoto M, Crossman J, Scribner K, Marsh T (2013) Microbial community assembly and succession on Lake sturgeon egg surfaces as a function of simulated spawning stream flow rate Microb. Ecol. 66:500–511. doi:10.1007/s00248-013-0256-6

    Article  PubMed  CAS  Google Scholar 

  20. Hentschel U, Schmid M, Wagner M, Fieseler L, Gernert C, Hacker J (2001) Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina Cavernicola FEMS Microbiol. Ecol. 35:305–312. doi:10.1111/j.1574-6941.2001.tb00816.x

    Article  PubMed  CAS  Google Scholar 

  21. Laport MS, Gandelman JFS, Muricy G, Giambiagi-deMarval M, George I (2016) Antagonistic interactions among bacteria isolated from either the same or from different sponges native to the Brazilian coast. J. Marine Sci. Res. Dev. 6(2). doi:10.4172/2155-9910.1000185

  22. Mangano S, Michaud L, Caruso C, Brilli M, Bruni V, Fani R, Lo Giudice A (2009) Antagonistic interactions between psychrotrophic cultivable bacteria isolated from Antarctic sponges: a preliminary analysis Res. Microbiol. 160:27–37

    Article  PubMed  CAS  Google Scholar 

  23. Rypien KL, Ward JR, Azam F (2010) Antagonistic interactions among coral-associated bacteria Environ. Microbiol. 12:28–39. doi:10.1111/j.1462-2920.2009.02027.x

    Article  PubMed  CAS  Google Scholar 

  24. Goldschmidt-Clermont E, Wahli T, Frey J, Burr SE (2008) Identification of bacteria from the normal flora of perch, Perca Fluviatilis L., and evaluation of their inhibitory potential towards Aeromonas species J. Fish Dis. 31:353–359. doi:10.1111/j.1365-2761.2008.00912.x

    Article  PubMed  CAS  Google Scholar 

  25. Spanggaard B, Huber I, Nielsen J, Sick EB, Pipper CB, Martinussen T, Slierendrecht WJ, Gram L (2001) The probiotic potential against vibriosis of the indigenous microflora of rainbow trout Environ. Microbiol. 3:755–765

    Article  PubMed  CAS  Google Scholar 

  26. Grossart H-P, Schlingloff A, Bernhard M, Simon M, Brinkhoff T (2004) Antagonistic activity of bacteria isolated from organic aggregates of the German Wadden Sea FEMS Microbiol. Ecol. 47:387–396. doi:10.1016/s0168-6496(03)00305-2

    Article  PubMed  CAS  Google Scholar 

  27. Lo Giudice A, Brilli M, Bruni V, De Domenico M, Fani R, Michaud L (2007) Bacterium–bacterium inhibitory interactions among psychrotrophic bacteria isolated from Antarctic seawater (Terra Nova Bay, Ross Sea) FEMS Microbiol. Ecol. 60:383–396. doi:10.1111/j.1574-6941.2007.00300.x

    Article  PubMed  CAS  Google Scholar 

  28. Long RA, Azam F (2001) Antagonistic interactions among marine pelagic bacteria Appl. Environ. Microbiol. 67:4975–4983. doi:10.1128/aem.67.11.4975-4983.2001

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Long RA, Rowley DC, Zamora E, Liu J, Bartlett DH, Azam F (2005) Antagonistic interactions among marine bacteria impede the proliferation of vibrio cholerae Appl. Environ. Microbiol. 71:8531–8536. doi:10.1128/aem.71.12.8531-8536.2005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Datta MS, Sliwerska E, Gore J, Polz MF, Cordero OX (2016) Microbial interactions lead to rapid micro-scale successions on model marine particles Nat. Commun. 7:11965. doi:10.1038/ncomms11965

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Yan L, Boyd KG, Adams DR, Burgess JG (2003) Biofilm-specific cross-species induction of antimicrobial compounds in bacilli Appl. Environ. Microbiol. 69:3719–3727. doi:10.1128/aem.69.7.3719-3727.2003

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Saha M, Ghosh D, Garai D, Jaisankar P, Sarkar KK, Dutta PK, Das S, Jha T, Mukherjee J (2005) Studies on the production and purification of an antimicrobial compound and taxonomy of the producer isolated from the marine environment of the Sundarbans Appl. Microbiol. Biotechnol. 66:497–505. doi:10.1007/s00253-004-1706-3

    Article  PubMed  CAS  Google Scholar 

  33. Evans J, Armstrong T-N (2006) Antagonistic interactions between honey bee bacterial symbionts and implications for disease BMC Ecol. 6:4

    Article  PubMed  PubMed Central  Google Scholar 

  34. Marín-Cevada V, Muñoz-Rojas J, Caballero-Mellado J, Mascarúa-Esparza MA, Castañeda-Lucio M, Carreño-López R, Estrada-de los Santos P, Fuentes-Ramírez LE (2012) Antagonistic interactions among bacteria inhabiting pineapple Appl. Soil Ecol. 61:230–235

    Article  Google Scholar 

  35. Rendueles O, Ghigo J-M (2012) Multi-species biofilms: how to avoid unfriendly neighbors FEMS Microbiol. Rev. 36:972–989. doi:10.1111/j.1574-6976.2012.00328.x

    Article  PubMed  CAS  Google Scholar 

  36. DeHaan PW, Libants SV, Elliott RF, Scribner KT (2006) Genetic population structure of remnant lake sturgeon populations in the upper Great Lakes basin Trans. Am. Fish. Soc. 135:1478–1492. doi:10.1577/t05-213.1

    Article  CAS  Google Scholar 

  37. Forsythe PS, Scribner KT, Crossman JA, Ragavendran A, Baker EA (2013) Experimental assessment of the magnitude and sources of lake sturgeon egg mortality in a natural stream setting Trans Am Fish Soc 142:1005–1011

    Article  Google Scholar 

  38. Forsythe PS, Scribner KT, Crossman JA, Ragavendran A, Baker EA, Davis C, Smith KK (2012) Environmental and lunar cues are predictive of the timing of river entry and spawning-site arrival in lake sturgeon Acipenser Fulvescens J. Fish Biol. 81:35–53. doi:10.1111/j.1095-8649.2012.03308.x

    Article  PubMed  CAS  Google Scholar 

  39. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary Genetics analysis (MEGA) software version 4.0 Mol. Biol. Evol. 24:1596–1599. doi:10.1093/molbev/msm092

    Article  PubMed  CAS  Google Scholar 

  40. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis Nucleic Acids Res. 37:D141–D145. doi:10.1093/nar/gkn879

    Article  PubMed  CAS  Google Scholar 

  41. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method Proc. Natl. Acad. Sci. U. S. A. 101:11030–11035. doi:10.1073/pnas.0404206101

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Mendoza L, Wilkens M, Urzúa A (1997) Antimicrobial study of the resinous exudates and of diterpenoids and flavonoids isolated from some Chilean Pseudognaphalium (Asteraceae) J. Ethnopharmacol. 58:85–88

    Article  PubMed  CAS  Google Scholar 

  43. R Development Core Team (2009) R: a launguage and environment for statistical computing. R foundation for Statistical Computing, Vienna

    Google Scholar 

  44. Loch TP, Faisal M (2010) Infection of lake whitefish (Coregonus Clupeaformis) with motile Aeromonas spp. in the Laurentian Great Lakes J. Great Lakes Res. 36:6–12

    Article  Google Scholar 

  45. Loch TP, Scribner K, Tempelman R, Whelan G, Faisal M (2012) Bacterial infections of Chinook salmon, Oncorhynchus Tshawytscha (Walbaum), returning to gamete collecting weirs in Michigan J. Fish Dis. 35:39–50. doi:10.1111/j.1365-2761.2011.01322.x

    Article  PubMed  CAS  Google Scholar 

  46. Faisal M, Loch T, Fujimoto M, Woodiga S, Eissa A, Honeyfield D, Wolgamood M, Walker E, Marsh T (2011) Characterization of novel Flavobacterium spp. involved in the mortality of Coho salmon (Oncorhynchus Kisutch) in their early life stages J Aquac Res Development S2:005

    Google Scholar 

  47. Brian, A, & Dawn, A (2007) Bacterial fish pathogens: diseases of farmed and wild fish. Springer Publishers, New York

  48. Merritt JH, Kadouri DE, O'Toole GA (2005) Growing and analyzing static biofilms Curr Protoc Microbiol 1B:1

    Google Scholar 

  49. Skyberg J, Siek K, Doetkott C, Nolan L (2007) Biofilm formation by avian Escherichia Coli in relation to media, source and phylogeny J. Appl. Microbiol. 102:548–554

    Article  PubMed  CAS  Google Scholar 

  50. Ellis AE (2001) Innate host defense mechanisms of fish against viruses and bacteria Dev. Comp. Immunol. 25:827–839. doi:10.1016/s0145-305x(01)00038-6

    Article  PubMed  CAS  Google Scholar 

  51. Magnadottir B (2006) Innate immunity of fish (overview) Fish & Shellfish Immunol 20:137–151. doi:10.1016/j.fsi.2004.09.006

    Article  CAS  Google Scholar 

  52. De la Fuente M, Vidal JM, Miranda CD, González G, Urrutia H (2013) Inhibition of Flavobacterium psychrophilum biofilm formation using a biofilm of the antagonist Pseudomonas Fluorescens FF48 SpringerPlus 2:1–9

    Article  CAS  Google Scholar 

  53. Gobeli S, Goldschmidt-Clermont E, Frey J, Burr SE (2009) Pseudomonas chlororaphis strain JF3835 reduces mortality of juvenile perch, Perca Fluviatilis L., caused by Aeromonas Sobria J. Fish Dis. 32:597–602. doi:10.1111/j.1365-2761.2009.01021.x

    Article  PubMed  CAS  Google Scholar 

  54. Korkea-aho T, Heikkinen J, Thompson K, von Wright A, Austin B (2011) Pseudomonas sp. M174 inhibits the fish pathogen Flavobacterium psychrophilum J. Appl. Microbiol. 111:266–277

    Article  PubMed  CAS  Google Scholar 

  55. Rao T (2010) Comparative effect of temperature on biofilm formation in natural and modified marine environment Aquat. Ecol. 44:463–478. doi:10.1007/s10452-009-9304-1

    Article  CAS  Google Scholar 

  56. Molobela I, Ilunga F (2012) Impact of bacterial biofilms: the importance of quantitative biofilm studies Ann Microbiol 62:461–467. doi:10.1007/s13213-011-0344-0

    Article  Google Scholar 

  57. Chadwick T, Wright P (1999) Nitrogen excretion and expression of urea cycle enzymes in the atlantic cod (Gadus Morhua l.): a comparison of early life stages with adults J. Exp. Biol. 202:2653–2662

    PubMed  CAS  Google Scholar 

  58. Steele SL, Chadwick TD, Wright PA (2001) Ammonia detoxification and localization of urea cycle enzyme activity in embryos of the rainbow trout (Oncorhynchus Mykiss) in relation to early tolerance to high environmental ammonia levels J. Exp. Biol. 204:2145–2154

    PubMed  CAS  Google Scholar 

  59. Granillo A, Canales M, Espíndola M, Rivera M, de Lucio V, Tovar A (2015) Antibiosis interaction of Staphylococccus aureus on aspergillus fumigatus assessed in vitro by mixed biofilm formation BMC Microbiol. 15:33

    Article  CAS  Google Scholar 

  60. Liebana R, Arregui L, Santos A, Murciano A, Marquina D, Serrano S (2016) Unravelling the interactions among microbial populations found in activated sludge during biofilm formation. FEMS Microbiol Ecol 92(9). doi:10.1093/femsec/fiw134

  61. Mehrabi Z, McMillan VE, Clark IM, Canning G, Hammond-Kosack KE, Preston G, Hirsch PR, Mauchline TH (2016) Pseudomonas spp. diversity is negatively associated with suppression of the wheat take-all pathogen Sci Rep 6:29905. doi:10.1038/srep29905

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Finlay BJ, Clarke KJ (1999) Ubiquitous dispersal of microbial species Nature 400:828

    Article  CAS  Google Scholar 

  63. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton,

    Google Scholar 

  64. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities Proc. Natl. Acad. Sci. U. S. A. 103:626–631

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Van der Gucht K, Cottenie K, Muylaert K, Vloemans N, Cousin S, Declerck S, Jeppesen E, Conde-Porcuna JM, Schwenk K, Zwart G, Degans H, Vyverman W, De Meester L (2007) The power of species sorting: local factors drive bacterial community composition over a wide range of spatial scales Proc. Natl. Acad. Sci. U. S. A. 104:20404–20409. doi:10.1073/pnas.0707200104

    Article  PubMed  PubMed Central  Google Scholar 

  66. Fraune S, Augustin R, Anton-Erxleben F, Wittlieb J, Gelhaus C, Klimovich VB (2010) In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides Proc. Natl. Acad. Sci. U. S. A. 107:18067–18072

    Article  PubMed  PubMed Central  Google Scholar 

  67. Fraune S, Augustin R, Bosch TCG (2011) Embryo protection in contemporary immunology: why bacteria matter Commun Integr Biol 4:369–372

    Article  PubMed  PubMed Central  Google Scholar 

  68. Zapien-Campos R, Olmedo-Alvarez G, Santillan M (2015) Antagonistic interactions are sufficient to explain self-assemblage of bacterial communities in a homogeneous environment: a computational modeling approach Front. Microbiol. 6:489. doi:10.3389/fmicb.2015.00489

    Article  PubMed  PubMed Central  Google Scholar 

  69. Madsen JS, Roder HL, Russel J, Sorensen H, Burmolle M, Sorensen SJ (2016) Coexistence facilitates interspecific biofilm formation in complex microbial communities Environ. Microbiol. 18:2565–2574. doi:10.1111/1462-2920.13335

    Article  PubMed  CAS  Google Scholar 

  70. Rivett DW, Scheuerl T, Culbert CT, Mombrikotb SB, Johnstone E, Barraclough TG, Bell T (2016) Resource-dependent attenuation of species interactions during bacterial succession ISME J 10:2259–2268. doi:10.1038/ismej.2016.11

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the hard work and dedication of our lake sturgeon field crew and colleagues: John Bauman, Katy Jay, Ryan Hastings, Jared Homola, and Edward Baker contributed to collection of gametes and hatchery operation. We thank the Michigan Department of Natural Resources, the Great Lakes Fishery Trust, Michigan Agricultural Experiment Station, the Center for Water Sciences and the WaterCube program at MSU, Sustainable Michigan Environmental Program, and a US Geological Survey grant to TLM for providing funding for this project. The authors have no conflict of interest to declare.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. L. Marsh.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fujimoto, M., Lovett, B., Angoshtari, R. et al. Antagonistic Interactions and Biofilm Forming Capabilities Among Bacterial Strains Isolated from the Egg Surfaces of Lake Sturgeon (Acipenser fulvescens). Microb Ecol 75, 22–37 (2018). https://doi.org/10.1007/s00248-017-1013-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-1013-z

Keywords

Navigation