Influence of Acidification and Warming of Seawater on Biofouling by Bacteria Grown over API 5L Steel

Abstract

The acidification and warming of seawater have several impacts on marine organisms, including over microorganisms. The influence of acidification and warming of seawater on biofilms grown on API 5L steel surfaces was evaluated by sequencing the 16S ribosomal gene. For this, three microcosms were designed, the first simulating the natural marine environment (MCC), the second with a decrease in pH from 8.1 to 7.9, and an increase in temperature by 2 °C (MMS), and the third with pH in around 7.7 and an increase in temperature of 4 °C (MES). The results showed that MCC was dominated by the Gammaproteobacteria class, mainly members of the Alteromonadales Order. The second most abundant group was Alphaproteobacteria, with a predominance of Rhodobacterales and Oceanospirillales. In the MMS system there was a balance between representatives of the Gammaproteobacteria and Alphaproteobacteria classes. In MES there was an inversion in the representations of the most prevalent classes previously described in MCC. In this condition, there was a predominance of members of the Alphaproteobacteria Class, in contrast to the decrease in the abundance of Gammaproteobacteria members. These results suggest that possible future climate changes may influence the dynamics of the biofouling process in surface metals.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. 1.

    Dlugokencky E, Tans P (2017) Trends in atmospheric carbon dioxide. National Oceanic & Atmospheric Administration, Earth System Research Laboratory. http://www.esrl.noaa.gov/gmd/ccgg/trends/global.html. Accessed 26 June 2020

  2. 2.

    Masson-Delmotte V, Zhai P, Pörtner HO, Roberts D, Skea J, Shukla PR, Pirani A, et al (2018) Global warming of 1.5°C: an IPCC special report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change. World Meteorological Organization, Geneva

  3. 3.

    Das S, Mangwani N (2015) Ocean acidification and marine microorganisms: responses and consequences. Oceanologia 59:349–361. https://doi.org/10.1016/j.oceano.2015.07.003

    Article  Google Scholar 

  4. 4.

    Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R et al (2004) The oceanic sink for anthropogenic CO2. Science 305(5682):367–371

    CAS  Article  Google Scholar 

  5. 5.

    Bates NR, Astor YM, Church MJ, Currie K, Dore JE, González-Dávila M, Lorenzoni L et al (2014) A time-series view of changing ocean chemistry due to ocean uptake of anthropogenic CO2 and ocean acidification. Oceanography 27(1):126–141. https://doi.org/10.5670/oceanog.2014.16

    Article  Google Scholar 

  6. 6.

    Friedrich T, Timmermann A, Abe-Ouchi A, Bates NR, Chikamoto MO, Church MJ, Dore JE et al (2012) Detecting regional anthropogenic trends in ocean acidification against natural variability. Nat Clim Change 2:167–171

    CAS  Article  Google Scholar 

  7. 7.

    Paul C, Sommer U, Garzke J, Moustaka-Gouni M, Paul A, Matthiessen B (2016) Effects of increased CO2 concentration on nutrient limited coastal summer plankton depend on temperature. Limnol Oceanog 61:853–868. https://doi.org/10.1002/lno.10256

    Article  Google Scholar 

  8. 8.

    Piontek J, Lunau M, Händel N, Borchard C, Wurst M, Engel A (2010) Acidification increases microbial polysaccharide degradation in the ocean. Biogeosciences 7:1615–1624

    CAS  Article  Google Scholar 

  9. 9.

    Pansch C, Nasrolahi A, Appelhans YS, Wahl M (2012) Impacts of ocean warming and acidification on the larval development of the barnacle Amphibalanus improvisus. J Exp Mar Biol Ecol 420–421:48–55. https://doi.org/10.1016/j.jembe.2012.03.023

    Article  Google Scholar 

  10. 10.

    Kushmaro A, Banin E, Loya Y, Stackebrandt E, Rosenberg E (2001) Vibrio shiloi sp. nov., the causative agent of bleaching of the coral Oculina patagonica. Int J Syst Evol Microbiol 51:1383–1388. https://doi.org/10.1099/00207713-51-4-1383

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Kimes NE, Grim CJ, Johnson WR, Hasan NA, Tall BD, Kothary MH, Kiss H et al (2012) Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. Isme J 6:835–846. https://doi.org/10.1038/ismej.2011.154

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Lindh MV, Riemann L, Baltar F, Romero-Oliva C, Salomon PS, Granéli E, Pinhassi J (2013) Consequences of increased temperature and acidification on bacterioplankton community composition during a mesocosm spring bloom in the Baltic Sea. Environ Microbiol Rep 5(2):252–262. https://doi.org/10.1111/1758-2229.12009

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    von Scheibner M, Dörge P, Biermann A, Sommer U, Hoppe HG, Jürgens K (2014) Impact of warming on phyto-bacterioplankton coupling and bacterial community composition in experimental mesocosms. Environ Microbiol 16(3):718–733. https://doi.org/10.1111/1462-2920.12195

    Article  Google Scholar 

  14. 14.

    Procópio L (2019) The role of biofilms in the corrosion of steel in marine environments. World J Microbiol Biotechnol 35(5):73. https://doi.org/10.1007/s11274-019-2647-4

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Capão A, Moreira-Filho P, Garcia M, Bitati S, Procópio L (2020) Marine bacterial community analysis on 316L stainless steel coupons by Illumina MiSeq sequencing. Biotechnol Lett 42(8):1431–1448. https://doi.org/10.1007/s10529-020-02927-9

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Enning D, Garrelfs J (2014) Corrosion of iron by sulfate-reducing bacteria: new views of an old problem. Appl Environ Microbiol 80:1226–1236. https://doi.org/10.1128/AEM.02848-13

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Enning D, Venzlaff H, Garrelfs J, Dinh HT, Meyer V, Mayrhofer K, Hassel AW, Stratmann M, Widdel F (2012) Marine sulfate-reducing bacteria cause serious corrosion of iron under electroconductive biogenic mineral crust. Environ Microbiol 14(7):1772–1787. https://doi.org/10.1111/j.1462-2920.2012.02778.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Kato S (2016) Microbial extracellular electron transfer and its relevance to iron corrosion. Microb Biotechnol 9(2):141–148. https://doi.org/10.1111/1751-7915.12340

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Emerson D (2019) The role of iron-oxidizing bacteris in biocorrosion: a review. Biofoouling 34:989–1000. https://doi.org/10.1080/08927014.2018.1526281

    CAS  Article  Google Scholar 

  20. 20.

    Dobretsov S (2010) Marine biofilms. In: Thomason JC (ed) Durr S. Biofouling, Wiley-Blackwell, pp 123–136

    Google Scholar 

  21. 21.

    Dobretsov S, Coutinho R, Rittschof D, Salta M, Ragazzola F, Hellio C (2019) The oceans are changing: impact of ocean warming and acidification on biofouling communities. Biofouling 35(5):585–595. https://doi.org/10.1080/08927014.2019.1624727

    Article  PubMed  Google Scholar 

  22. 22.

    Procópio L (2020) The era of “omics” technologies in the study of microbiologically influenced corrosion. Biotechnol Lett 42(3):341–356. https://doi.org/10.1007/s10529-019-02789-w

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Lau SCK, Thiyagarajan V, Cheung SCK, Qian P (2005) Roles of bacterial community composition in biofilms as a mediator for larval settlement of three marine invertebrates. Aquat Microb Ecol 38:41–51. https://doi.org/10.3354/ame038041

    Article  Google Scholar 

  24. 24.

    Whalan S, Webster NS (2014) Sponge larval settlement cues: the role of microbial biofilms in a warming ocean. Sci Rep. https://doi.org/10.1038/srep04072

    Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Patil SA, Harnisch F, Koch C, Hubschmann T, Fetzer I, Carmona-Martınez AA, M€uller S, Schruoder U, (2011) Electroactive mixed culture derived biofilms in microbial bioelectrochemical systems: the role of pH on biofilm formation, performance and composition. Bioresour Technol 102:9683–9690. https://doi.org/10.1016/j.biortech.2011.07.087

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Peck LS, Clark MS, Power D, Reis J, Batista FM, Harper EM (2015) Acidification effects on biofouling communities: winners and losers. Glob Change Biol 21:1907–1913. https://doi.org/10.1111/gcb.12841

    Article  Google Scholar 

  27. 27.

    Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD et al (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742. https://doi.org/10.1126/science.1152509

    CAS  Article  Google Scholar 

  28. 28.

    Witt V, Wild C, Anthony KR, Diaz-Pulido G, Uthicke S (2011) Effects of ocean acidification on microbial community composition of, and oxygen fluxes through, biofilms from the Great Barrier Reef. Environ Microbiol 13(11):2976–2989. https://doi.org/10.1111/j.1462-2920.2011.02571.x

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Okazaki RR, Towle EK, van Hooidonk R, Mor C, Winter RN, Piggot AM, Cunning R et al (2017) Species-specific responses to climate change and community composition determine future calcification rates of Florida Keys reefs. Glob Chang Biol 23:1023–1035. https://doi.org/10.1111/gcb.13481

    Article  PubMed  Google Scholar 

  30. 30.

    Kerfahi D, Harvey BP, Agostini S, Kon K, Huang R, Adams JM, Hall-Spencer JM (2020) Responses of intertidal bacterial biofilm communities to increasing pCO2. Mar Biotechnolr. https://doi.org/10.1007/s10126-020-09958-3

    Article  Google Scholar 

  31. 31.

    Nelson KS, Baltar F, Lamare MD, Morales SE (2020) Ocean acidification affects microbial community and invertebrate settlement on biofilms. Sci Rep 10(1):3274. https://doi.org/10.1038/s41598-020-60023-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    de Brito LV, Coutinho R, Cavalcanti EH, Benchimol M (2007) The influence of macrofouling on the corrosion behaviour of API 5L X65 carbon steel. Biofouling 23(3–4):193–201. https://doi.org/10.1080/08927010701258966

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Procópio L (2020) Changes in microbial community in the presence of oil and chemical dispersant and their effects on the corrosion of API 5L steel coupons in a marine-simulated microcosm. Appl Microbiol Biotechnol 104(14):6397–6411. https://doi.org/10.1007/s00253-020-10688-8

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    Wang Y, Qian PY (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS ONE 4(10):e7401. https://doi.org/10.1371/journal.pone.0007401

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6(3):610–618. https://doi.org/10.1038/ismej.2011.139

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palae Electro 4(1):1–9

    Google Scholar 

  37. 37.

    McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8(4):e61217. https://doi.org/10.1371/journal.pone.0061217

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Oksanen J, Guillaume BF, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, et al. (2019) vegan: Community Ecology Package. R package version 2.5-6.

  39. 39.

    Tang Y, Horikoshi M, Li W (2016) ggfortify: Unified Interface to Visualize Statistical Results of Popular R Packages. The R Journal 8:474–485

    Article  Google Scholar 

  40. 40.

    R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  41. 41.

    York A (2018) Marine biogeochemical cycles in a changing world. Nat Rev Microbiol 16:259. https://doi.org/10.1038/nrmicro.2018.40

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    Jansson JK, Hofmockel KS (2020) Soil microbiomes and climate change. Nat Rev Microbiol 18:35–46. https://doi.org/10.1038/s41579-019-0265-7

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Hurd CL, Lenton A, Tilbrook B, Boyd PW (2017) Current understanding and challenges for oceans in a higher-CO2 world. Nat Clim Change 8:686–694. https://doi.org/10.1038/s41558-018-0211-0

    CAS  Article  Google Scholar 

  44. 44.

    Hutchins DA, Fu F (2017) Microorganisms and ocean global change. Nat Microbiol 2:17058. https://doi.org/10.1038/nmicrobiol.2017.58

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Hare CE, Leblanc K, DiTullio GR, Kudela RM, Zhang Y, Lee PA, Riseman S, Hutchins DA (2007) Consequences of increased temperature and CO2 for phytoplankton community structure in the Bering Sea. Mar Ecol Prog Ser 352:9–16. https://doi.org/10.3354/meps07182

    CAS  Article  Google Scholar 

  46. 46.

    Thomas MK, Kremer CT, Klausmeier CA, Litchman E (2012) A global pattern of thermal adaptation in marine phytoplankton. Science 338(6110):1085–1088. https://doi.org/10.1126/science.1224836

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Tatters AO, Roleda MY, Schnetzer A, Fu F, Hurd CL, Boyd PW, Caron DA, Lie AA, Hoffmann LJ, Hutchins DA (2013) Short- and long-term conditioning of a temperate marine diatom community to acidification and warming. Philos Trans R Soc Lond B Biol Sci 368(1627):20120437. https://doi.org/10.1098/rstb.2012.0437

    Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Kerfahi D, Harvey BP, Agostini S, Kon K, Huang R, Adams JM, Hall-Spencer J (2020) Responses of Intertidal Bacterial Biofilm Communities to Increasing pCO2. Mar Biotechnol 22(6):727–738. https://doi.org/10.1007/s10126-020-09958-3

    CAS  Article  Google Scholar 

  49. 49.

    IPCC (2014) Climate change 2014. In: Pachauri RK, Meyer LA (ed) Synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change, Geneva, p 151

  50. 50.

    Lidbury I, Johnson V, Hall-Spencer JM, Munn CB, Cunliffe M (2012) Community-level response of coastal microbial biofilms to ocean acidification in a natural carbon dioxide vent ecosystem. Mar Pollut Bull 64(5):1063–1066. https://doi.org/10.1016/j.marpolbul.2012.02.011

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    Taylor JD, Ellis R, Milazzo M, Hall-Spencer JM, Cunliffe M (2014) Intertidal epilithic bacteria diversity changes along a naturally occurring carbon dioxide and pH gradient. FEMS Microbiol Ecol 89:670–678

    CAS  Article  Google Scholar 

  52. 52.

    Currie AR, Tait K, Parry H, de Francisco-Mora B, Hicks N, Osborn AM, Widdicombe S, Stahl H (2017) Marine microbial gene abundance and community composition in response to ocean acidification and elevated temperature in two contrasting coastal marine sediments. Front Microbiol 8:1599. https://doi.org/10.3389/fmicb.2017.01599

    Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Smale DA, Taylor JD, Coombs SH, Moore G, Cunliffe M (2017) Community responses to seawater warming are conserved across diverse biological groupings and taxonomic resolutions. Proc Biol Sci 284(1862):20170534. https://doi.org/10.1098/rspb.2017.0534

    Article  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Russell BD, Connell SD, Findlay HS, Tait K, Widdicombe S, Mieszkowska N (2013) Ocean acidification and rising temperatures may increase biofilm primary productivity but decrease grazer consumption. Philos Trans R Soc Lond B Biol Sci 368(1627):20120438. https://doi.org/10.1098/rstb.2012.0438

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Krause E, Wichels A, Giménez L, Lunau M, Schilhabel MB, Gerdts G (2012) Small changes in pH have direct effects on marine bacterial community composition: a microcosm approach. PLoS ONE 7(10):e47035. https://doi.org/10.1371/journal.pone.0047035

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Hassenrück C, Fink A, Lichtschlag A, Tegetmeyer HE, de Beer D, Ramette A (2016) Quantification of the effects of ocean acidification on sediment microbial communities in the environment: the importance of ecosystem approaches. FEMS Microbiol Ecol 92(5):fiw27. https://doi.org/10.1093/femsec/fiw027

    CAS  Article  Google Scholar 

  57. 57.

    Meron D, Rodolfo-Metalpa R, Cunning R, Baker AC, Fine M, Banin E (2012) Changes in coral microbial communities in response to a natural pH gradient. ISME J 6(9):1775–1785. https://doi.org/10.1038/ismej.2012.19

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Luciano Procópio.

Ethics declarations

Conflict of interest

There is no conflict of interest declared.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 207 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lamim, V.B., Procópio, L. Influence of Acidification and Warming of Seawater on Biofouling by Bacteria Grown over API 5L Steel. Indian J Microbiol (2021). https://doi.org/10.1007/s12088-021-00925-7

Download citation

Keywords

  • Acidification
  • Warming
  • Seawater
  • Biofouling
  • API 5L steel
  • Metagenome