Skip to main content

Growth Patterns of Giant Deep Sea Beggiatoaceae from a Guaymas Basin Vent Site

  • Chapter
  • First Online:
Marine Hydrocarbon Seeps

Part of the book series: Springer Oceanography ((SPRINGEROCEAN))

  • 701 Accesses

Abstract

We studied the growth of giant filamentous sulfur oxidizing bacteria of the family Beggiatoaceae collected from a hydrothermal seep area in the Guaymas Basin. We measured the incorporation of 14C-bicarbonate tracer into individual filaments using a microimager that allows quantitative determination of the distribution of radioisotopes with 20 µm resolution. Filaments incorporated label along their entire length; thus growth occurred uniformly throughout these whole filaments and not only at their tips. Uptake of 14C-bicarbonate was strongly stimulated by reducing the pH from 8.2, the value near the sediment surface, to 7.05, as found within 1–2 mm below the surface; the presence of oxygen or sulfide had no effect. Thus, Beggiatoaceae strongly prefer assimilation of CO2 over other DIC species. In consequence, migration of these motile filaments into deeper sediments, where sharply decreasing pH increases the availability of CO2, will favor cell growth. Genomic evidence was found for periplasmic carbonic anhydrases, indicative of the carbon concentration mechanism.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 139.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Bendtsen JD, Kiemer L, Fausbøll A, Brunak S (2005) Non-classical protein secretion in bacteria. BMC Microbiol 5:58–70

    Article  Google Scholar 

  • de Beer D, Sauter E, Niemann H, Kaul N, Foucher JP, Witte U, Schlüter M, Boetius A (2006) In situ fluxes and zonation of microbial activity in surface sediments of the Håkon Mosby Mud Volcano. Limnol Oceanogr 51(3):1315–1331

    Article  Google Scholar 

  • Dobrinski KP, Boller AJ, Scott KM (2010) Expression and function of four carbonic anhydrase homologs in the deep-sea chemolithoautotrophc Thiomicrospira crunogena. Appl Environ Microbiol 76:3561–3567

    Article  Google Scholar 

  • Dombrowski N, Seitz KW, Teske AP, Baker BJ (2017) Genomic insights into potential interdependencies in microbial hydrocarbon and nutrient cycling in hydrothermal sediments. Microbiome 5:106

    Article  Google Scholar 

  • Hagen KD, Nelson DC (1997) Use of reduced sulfur compounds by Beggiatoa spp.: enzymology and physiology of marine and freshwater strains in homogeneous and gradient cultures. Appl Environ Microbiol 63:3957–3964

    Article  Google Scholar 

  • Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

    Article  Google Scholar 

  • Li T, Sharp C, Ataeian M, Strous M, de Beer D (2018) Role of extracellular carbonic anhydrase in dissolved inorganic carbon uptake in alkaliphilic phototrophic biofilm. Front Microbiol 9:2490

    Article  Google Scholar 

  • MacGregor BJ (2016) Visualizing evolutionary relationships of multidomain proteins: an example from receiver (REC) domains of sensor histidine kinases in the Candidatus Maribeggiatoa str. Orange Guaymas Draft Genome. Front Microbiol 7:1780

    Article  Google Scholar 

  • Marchler-Bauer A, Bo Y, Han LY, He JE, Lanczycki CJ, Lu SN, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang ZX, Yamashita RA, Zhang DC, Zheng CJ, Geer LY, Bryant SH (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45(D1):D200–D203

    Article  Google Scholar 

  • McHatton SC, Barry JP, Jannasch HW, Nelson DC (1996) Nigh nitrate concentrations in vacuolate, autotrophic marine Beggiatoa spp. Appl Environ Microbiol 62:954–958

    Article  Google Scholar 

  • McKay LJ, MacGregor BJ, Biddle JF, Mendlovitz HP, Hoer D, Lipp JS, Lloyd KG, Teske AP (2012) Spatial heterogeneity and underlying geochemistry of phylogenetically diverse orange and white Beggiatoa mats in Guaymas Basin hydrothermal sediments. Deep-Sea Res Part 1 67:21–31

    Article  Google Scholar 

  • McKay LJ, Klokman VW, Mendlovitz HP, LaRowe DE, Hoer D, Albert DB, Amend JP, Teske A (2016) Thermal and geochemical influences on microbial biogeography in the hydrothermal sediments of Guaymas Basin, Gulf of California. Environ Microbiol Rep 8:150–161

    Article  Google Scholar 

  • Mezzino M, Strohl WR, Larkin JM (1984) Characterization of Beggiatoa alba. Arch Microbiol 137:139–144

    Article  Google Scholar 

  • Nelson DC, Castenholz RW (1981) Organic nutrition by Beggiatoa sp. J Bact 147:236–247

    Article  Google Scholar 

  • Nelson DC, Hagen KD (1995) Physiology and biochemistry of symbiotic and free-living chemoautotrophic sulfur bacteria. Am Zool 35:91–101

    Article  Google Scholar 

  • Nelson DC, Jannasch HW (1983) Chemoautotrophic growth of a marine Beggiatoa in sulfide-gradient cultures. Arch Microbiol 136:262–269

    Article  Google Scholar 

  • Nelson DC, Jørgensen BB, Revsbech NP (1986a) Growth pattern and yield of a chemoautotrophic Beggiatoa sp. in oxygen-sulfide microgradients. Appl Environ Microbiol 52:225–233

    Article  Google Scholar 

  • Nelson DC, Revsbech NP, Jørgensen BB (1986b) Microoxic-anoxic niche of Beggiatoa spp.: microelectrode survey of marine and freshwater strains. Appl Environ Microbiol 52:161–168

    Article  Google Scholar 

  • Nelson DC, Wirsen CO, Jannasch HW (1989) Characterization of large, autotrophic Beggiatoa spp. abundant at hydrothermal vents of the Guaymas Basin. Appl Environ Microbiol 55:2909–2917

    Article  Google Scholar 

  • Otte S, Kuenen JG, Nielsen LP, Paerl HW, Zopfi J, Schulz HN, Teske A, Strotmann B, Gallardo VA, Jørgensen BB (1999) Nitrogen, carbon, and sulfur metabolism in natural Thioploca samples. Appl Environ Microbiol 65:3148–3157

    Article  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8(10):785–786

    Article  Google Scholar 

  • Preisler A, de Beer D, Lichtschlag A, Lavik G, Boetius A, Jørgensen BB (2007) Biological and chemical sulfide oxidation in a Beggiatoa inhabited marine sediment. ISME J 1:341–353

    Article  Google Scholar 

  • Salman V, Amann R, Girnth A-C, Polerecky L, Bailey J, Høgslund S, Jessen G, Pantoja S, Schulz-Vogt HN (2011) A single-cell sequencing approach to the classification of large, vacuolated sulfur bacteria. Syst Appl Microbiol 34:243–259

    Article  Google Scholar 

  • Schutte C, Teske A, MacGregor B, Salman-Carvalho V, Lavik G, Hach P, deBeer D (2018) Filamentous giant Beggiatoaceae from Guaymas Basin are capable of both denitrification and dissimilatory nitrate reduction to ammonium (DNRA). Appl Environ Microbiol 84:e02860-17

    Article  Google Scholar 

  • Strohl WR, Larkin JM (1978) Cell division and trichome breakage in Beggiatoa. Curr Microbiol 1:151–155

    Article  Google Scholar 

  • Sweerts J-PRA, de Beer D, Nielsen LP, Verdouw H, van den Heuvel JC, Cohen Y, Cappenberg TE (1990) Denitrification by sulphur oxidizing Beggiatoa spp. mats on freshwater sediments. Nature 344:762–763

    Article  Google Scholar 

  • Tchernov D, Hassidim M, Luz B, Sukenik A, Reinhold L, Kaplan A (1997) Sustained net CO2 evolution during photosynthesis by marine microorganism. Curr Biol 7:723–728

    Article  Google Scholar 

  • Teske A, Nelson DC (2006) The genera Beggiatoa and Thioploca. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The Prokaryotes, vol 6. Springer, New York, pp 784–810

    Chapter  Google Scholar 

  • Teske A, Salman V (2014) The family Beggiatoaceae. In: Rosenberg E, DeLong EF, Thompson F, Lory S, Stackebrandt E (eds) The Prokaryotes—Gammaproteobacteria. The Prokaryotes, 4th edn. Springer, Berlin, pp 93–134

    Google Scholar 

  • Teske A, de Beer D, McKay LJ, Tivey MK, Biddle JF, Hoer D, Lloyd KG, Lever MA, Røy H, Albert DB, Mendlovitz HP, MacGregor BJ (2016) The Guaymas Basin hiking guide to hydrothermal mounds, chimneys, and microbial mats: complex seafloor expressions of subsurface hydrothermal circulation. Front Microbiol 7:1–23

    Article  Google Scholar 

  • Van Gaever S, Moodley L, de Beer D, Vanreusel A (2006) Meiobenthos at the Arctic Håkon Mosby Mud Volcano, with a parental-caring nematode thriving in sulphide-rich sediments. Mar Ecol Prog Ser 321:143–155

    Article  Google Scholar 

  • Wu Y, Gao K, Riebesell U (2010) CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7:2915–2923

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful for the excellent jobs done by the Alvin team and the R/V Atlantis crew during cruise AT37-06. Dirk de Beer’s and Charles Schutte’s cruise participation was financed by the Max-Planck-Society in Munich, Germany. The cruise was supported by NSF-Biological Oceanography (NSF-OCE 1357238).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dirk de Beer .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

de Beer, D., Ferdelman, T., MacGregor, B.J., Teske, A., Schutte, C.A. (2020). Growth Patterns of Giant Deep Sea Beggiatoaceae from a Guaymas Basin Vent Site. In: Teske, A., Carvalho, V. (eds) Marine Hydrocarbon Seeps. Springer Oceanography. Springer, Cham. https://doi.org/10.1007/978-3-030-34827-4_9

Download citation

Publish with us

Policies and ethics