, Volume 123, Issue 1–2, pp 117–133 | Cite as

Concentrations, turnover rates and fluxes of polyamines in coastal waters of the South Atlantic Bight

  • Qian Liu
  • Xinxin Lu
  • Bradley B. Tolar
  • Xiaozhen Mou
  • James T. Hollibaugh


Polyamines are short-chain aliphatic compounds containing multiple amine groups. They are important components of the cytosol of eukaryotes and are present at mmol L−1 concentrations inside phytoplankton cells, while complex polyamines play a role in biosilica deposition. Concentrations of polyamines measured in seawater are typically in the sub-nmol L−1 range, implying rapid and efficient uptake by osmotrophs, likely bacterioplankton. We measured turnover rates of three polyamines (putrescine, spermidine and spermine) using 3H-labeled compounds and determined their concentrations by HPLC to estimate polyamine contributions to dissolved organic matter and bacterioplankton carbon and nitrogen demand. These measurements were made on transects from the inner shelf to the Gulf Stream across the South Atlantic Bight (SAB) during April and October of 2011 and in salt marsh estuaries on the Georgia coast during August of 2011 and April of 2012. We found that turnover rates of polyamines were similar to those of amino acids (arginine and glutamic acid) measured in the same samples; however, fluxes of polyamines into bacterioplankton were much lower than amino acid fluxes as a result of low ambient concentrations. Turnover rates and fluxes of polyamines decreased from near-shore waters to the shelf-break, following the pattern of chlorophyll a concentration. Polyamine uptake accounted for less than 10 % of bacterial N demand and 5 % of bacterial C demand on average, with a large variation among water masses.


Polyamines Dissolved organic nitrogen Bacterioplankton Spermidine Spermine Putrescine DFAA South Atlantic Bight 



We thank the captain and crew of the R/V Savannah for their assistance with sample collection during two cruises, as well as Anna M. Bratcher for assisting with processing the nutrient data presented here. We would also like to thank the crew of the R/V Salty Dawg, especially Jacob Shalack, for assistance with sample collections at GCE-LTER sites, as well as Mary Price and Gracie Townsend for helping with facilities and equipment at UGAMI. This research was funded by the National Science Foundation (NSF OCE 1029742 to J.T.H and OCE 1029607 to X.M.).

Supplementary material

10533_2014_56_MOESM1_ESM.docx (18 kb)
Supplementary material 1 (DOCX 18 kb)
10533_2014_56_MOESM2_ESM.pdf (1001 kb)
Fig. S1 (a) Stations sampled during April (18–22) and October (2–6) cruises in the South Atlantic Bight (SAB). Stations visited on both cruises are represented with diamonds (purple); stations visited only on the April cruise represented with squares (blue) and those visited only on the October cruise represented with circles (red). (b) GCE-LTER sites located on the central Georgia coast and bounded on the east by the SAB. Samples were collected from the Sapelo Sound (SP, GCE 1, 2 and 3), Marsh Landing (ML) and Altamaha Sound (AL, GCE 7, 8 and 9) during 13–16 August 2011 and 17–20 April 2012. Fig. S2 Relative fluorescence (mg m−3), concentrations of biogenic silica (BSi, µmol L−1), l-leucine incorporation rates (LEU, pmol h−1 L−1) and bacterial 16S rRNA gene abundance (copies L−1) in samples collected on the April (a, b) and October (c, d) cruises. Numbers on the abscissa identify the station as per Figure S1a. SW, surface water; MW, mid-water; BW, bottom water (PDF 1001 kb)


  1. Agustí S, Duarte CM (2013) Phytoplankton lysis predicts dissolved organic carbon release in marine plankton communities. Biogeosciences 10:1259–1264CrossRefGoogle Scholar
  2. Alcázar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876CrossRefGoogle Scholar
  3. Azam F, Frenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263CrossRefGoogle Scholar
  4. Badini L, Pistocchi R, Bagni N (1994) Polyamine transport in the seaweed Ulva Rigida (Chlorophyta). J Phycol 30:599–605CrossRefGoogle Scholar
  5. Bagni N, Calzoni GL, Speranza A (1978) Polyamines as sole nitrogen sources for Helianthus Tuberosus explants in vitro. New Phytol 80:317–323CrossRefGoogle Scholar
  6. Bano N, Hollibaugh JT (2000) Diveristy and distribution of DNA sequences with affinity to ammonia-oxidizing bacteria of the beta subdivision of the class Proteobacteria in the Arctic Ocean. Appl Environ Microbiol 66:1960–1969Google Scholar
  7. Bridoux MC, Ingalls AE (2010) Structural identification of long-chain polyamines associated with diatom biosilica in a Southern Ocean sediment core. Geochim Cosmochim Acta 74:4044–4057CrossRefGoogle Scholar
  8. Brzezinski MA, Nelson DM (1989) Seasonal changes in the silicon cycle within a Gulf Stream warm-core ring. Deep-Sea Res 36:1009–1030CrossRefGoogle Scholar
  9. Brzezinski MA, Phillips DR, Chavez FP, Friederich GE, Dugdale RC (1997) Silica production in the Monterey, California, upwelling system. Limnol Oceanogr 42(8):1694–1705CrossRefGoogle Scholar
  10. Buchan A, Hadden M, Suzuki MT (2009) Development and application of quantitative-PCR tools for subgroups of the Roseobacter clade. Appl Environ Microbiol 75:7542–7547CrossRefGoogle Scholar
  11. Conover RJ (1966) Feeding on large particles by Calanus hyperboreus. In: Barnes H (ed) Some Contemporary Studies in Marine Science. George Allen and Unwin Ltd., London, pp 187–194Google Scholar
  12. Cottrell MT, Suttle CA (1995) Dynamics of a lytic virus infecting the photosynthetic marine picoflagellate Micromonas pusilla. Limnol Oceanogr 40:730–739CrossRefGoogle Scholar
  13. Crawford CC, Hobbie JE, Webb KL (1974) The utilization of dissolved free amino acids by estuarine microorganisms. Ecology 55:551–563CrossRefGoogle Scholar
  14. Denger K, Smits THM, Cook AM (2006) Genome-enabled analysis of utilization of taurine as sole source of carbon or of nitrogen by Rhodobacter sphaeroides 2.4. 1. Microbiology 152:3197–3206CrossRefGoogle Scholar
  15. Ducklow HW, Steinberg DK, Buesseler KO (2001) Upper ocean carbon export and the biological pump. Oceanography 14:50–58CrossRefGoogle Scholar
  16. Ferguson RL, Sunda WG (1984) Utilization of amino acids by planktonic marine bacteria: importance of clean technique and low substrate additions. Limnol Oceanogr 29:258–274CrossRefGoogle Scholar
  17. Fuell C, Elliott KA, Hanfrey CC, Franceschetti M, Michael AJ (2010) Polyamine biosynthetic diversity in plants and algae. Plant Physiol Biochem 48:513–520CrossRefGoogle Scholar
  18. Fuhrman J (1987) Close coupling between release and uptake of dissolved free amino acids in seawater studied by an isotope dilution approach. Mar Ecol Prog Ser 37:45–52CrossRefGoogle Scholar
  19. Fuhrman J (1990) Dissolved free amino acids cycling in an estuarine outflow plume. Mar Ecol Prog Ser 66:197–203CrossRefGoogle Scholar
  20. Goldman JC, Dennett MR (1991) Ammonium regeneration and carbon utilization by marine bacteria grown on mixed substrates. Mar Biol 109:369–378CrossRefGoogle Scholar
  21. Goldman JC, Caron DA, Dennett MR (1987) Regulation of gross growth efficiency and ammonium regeneration in bacteria by substrate C:N ratio. Limnol Oceanogr 32:1239–1252CrossRefGoogle Scholar
  22. Hamana K, Matsuzaki S (1982) Widespread occurrence of norspermidine and norspermine in eukaryotic Algae. J Biochem 91(4):1321–1328Google Scholar
  23. Hamana K, Matsuzaki S (1985) Further study on polyamines in primitive unicellular eukaryotic algae. J Biochem 97:1311–1315Google Scholar
  24. Hamana K, Matsuzaki S (1992) Polyamines as a chemotaxonomic marker in bacterial systematics. Crit Rev Microbiol 18:261–283CrossRefGoogle Scholar
  25. Hasegawa T, Koike I, Mukai H (2001) Fate of food nitrogen in marine copepods. Mar Ecol Prog Ser 210:167–174CrossRefGoogle Scholar
  26. Hobbie JE, Crawford CC (1969) Respiration corrections for bacterial uptake of dissolved organic compounds in natural waters. Limnol Oceanogr 14:528–532CrossRefGoogle Scholar
  27. Hobbie JE, Crawford CC, Webb KL (1968) Amino acid flux in an estuary. Science 159:1463–1464CrossRefGoogle Scholar
  28. Höfle MG (1984) Degradation of putrescine and cadaverine in seawater cultures by marine bacteria. Appl Environ Microbiol 47:843–849Google Scholar
  29. Hollibaugh JT (1978) Nitrogen regeneration during the degradation of several amino acids by plankton communities collected near Halifax, Nova Scotia, Canada. Mar Biol 45:191–201CrossRefGoogle Scholar
  30. Hollibaugh JT, Wong PS (1992) Ethanol-extractable substrate pools and the incorporation of thymidine, l-leucine, and other substrates by bacterioplankton. Can J Microbiol 38:605–613CrossRefGoogle Scholar
  31. Holmes RM, Aminot A, Kerouel R, Hooker BA, Peterson BJ (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 56:1801–1808CrossRefGoogle Scholar
  32. Igarashi K, Kashiwagi K (1999) Polyamine transport in bacteria and yeast. Biochem J 344:633–642CrossRefGoogle Scholar
  33. Incharoensakdi A, Jantaro S, Raksajit W, Mäenpää P (2010) Polyamines in cyanobacteria: biosynthesis, transport and abiotic stress. In: Méndez-Vilas A (ed) Current research, technology and education topics in applied microbiology and microbial biotechnology. Formatex, Badajoz, pp 23–32Google Scholar
  34. Jantaro S, Mäenpää P, Mulo P, Incharoensakdi A (2003) Content and biosynthesis of polyamines in salt and osmotically stressed cells of Synechocystis sp. PCC 6803. FEMS Microbiol Lett 228:129–135CrossRefGoogle Scholar
  35. Jones MN (1984) Nitrate reduction by shaking with cadmium: alternative to cadmium columns. Water Res 18(5):643–646CrossRefGoogle Scholar
  36. Kirchman DL, K’nees E, Hodson R (1985) Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Appl Environ Microbiol 49:599–607Google Scholar
  37. Körös Á, Varga Z, Molnár-Perl I (2008) Simulatneous analysis of amino acids and amines as their o-phthalaldehyde-ethanediol-9-fluorenylmethyl chloroformate derivatives in cheese by high-performance liquid chromatography. J Chromatogr A 1203:146–152CrossRefGoogle Scholar
  38. Kröger N, Deutzmann R, Bergsdorf C, Sumper M (2000) Species-specific polyamines from diatoms control silica morphology. PNAS 97:14133–14138CrossRefGoogle Scholar
  39. Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) Advances in polyamine research in 2007. J Plant Res 120:345–350CrossRefGoogle Scholar
  40. Lampert W (1978) Release of dissolved organic carbon by grazing zooplankton. Limnol Oceanogr 23:831–834CrossRefGoogle Scholar
  41. Lee C (1992) Controls on organic carbon preservation: the use of stratified water bodies to compare intrinsic rates of decomposition in oxic and anoxic systems. Geochim Cosmochim Acta 56:3323–3335CrossRefGoogle Scholar
  42. Lee C, Jørgensen NOG (1995) Seasonal cycling of putrescine and amino acids in relation to biological production in a stratified coastal salt pond. Biogeochemistry 29:131–157CrossRefGoogle Scholar
  43. Legendre P, Legendre L (2012) Numerical ecology, vol 24, 3rd edn. Elsevier, New YorkGoogle Scholar
  44. Lin S, Zou T, Gao H, Guo X (2009) The vertical attenuation of irradiance as a function of turbidity: a case of the Huanghai (Yellow) Sea in spring. Acta Oceanol Sin 28(5):66–75Google Scholar
  45. Lu Y, Hwang D (2002) Polyamine profile in the paralytic shellfish poison-producing alga Alexandrium minutum. J Plankton Res 24(3):275–279CrossRefGoogle Scholar
  46. Lu X, Zou L, Clevinger C, Liu Q, Hollibaugh JT, Mou X (2014) Temporal dynamics and depth variations of dissolved free amino acids and polyamines in coastal seawater determined by high-performance liquid chromatography. Mar Chem 163:36–44CrossRefGoogle Scholar
  47. Marián FD, García-Jiménez P, Robaina RR (2000) Polyamines in marine macroalgae: levels of putrescine, spermidine and spermine in the thalli and changes in their concentration during glycerol-induced cell growth in vitro. Physiol Plant 110:530–534CrossRefGoogle Scholar
  48. Moran MA, Belas R, Schell MA, González JM, Sun F, Sun S et al (2007) Ecological genomics of marine roseobacters. Appl Environ Microbiol 73:4559–4569CrossRefGoogle Scholar
  49. Mou X, Sun S, Rayapati P, Moran MA (2010) Genes for transport and metabolism of spermidine in Ruegeria pomeroyi DSS-3 and other marine bacteria. Aquat Microb Ecol 58:311–321CrossRefGoogle Scholar
  50. Mou X, Vila-Costa M, Sun S, Zhao W, Sharma S, Moran MA (2011) Metatranscriptomic signature of exogenous polyamines utilization by coastal bacterioplankton. Environ Microbiol Rep 3:798–806CrossRefGoogle Scholar
  51. Nelson DM, Tréguer P, Brzezinski MA, Leynaert A, Queguiner B (1995) Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Glob Biogeochem Cycle 9:359–372CrossRefGoogle Scholar
  52. Nishibori N, Nishijima T (2007) Changes in polyamine levels during growth of a red-tide causing phytoplankton Chattonella antiqua (Raphidophyceae). Eur J Phycol 39:51–55CrossRefGoogle Scholar
  53. Nishibori N, Nishii A, Takayama H (2001a) Detection of free polyamine in coastal seawater using ion exchange chromatography. ICES J Mar Sci 58:1201–1207CrossRefGoogle Scholar
  54. Nishibori N, Yuasa A, Sakai M, Fujihara S, Nishio S (2001b) Free polyamine concentrations in coastal seawater during phytoplankton bloom. Fish Sci 67:79–83CrossRefGoogle Scholar
  55. Nishibori N, Matuyama Y, Uchida T, Moriyama T, Ogita Y, Oda M, Hirota H (2003) Spatial and temporal variations in free polyamine distributions in Uranouchi Inlet, Japan. Mar Chem 82(3):307–314CrossRefGoogle Scholar
  56. Nishibori N, Fujihara S, Nishijima T (2006) Changes in intracellular polyamine concentration during growth of Heterosigma akashiwo (Raphidophyceae). Fish Sci 72:350–355CrossRefGoogle Scholar
  57. Paasche E (1973) Silicon and the ecology of marine planktonic diatoms. 1. Thalassiosira pseudonana (Cyclotella nana) grown in chemostats with silicate as the limiting nutrient. Mar Biol 19:117–126CrossRefGoogle Scholar
  58. Rastogi R, Davies PJ (1990) Polyamine metabolism in ripening tomato fruit. Plant Physiol 94:1449–1455CrossRefGoogle Scholar
  59. Simon M, Azam F (1989) Protein content and protein synthesis rates of planktonic Marine bacteria. Mar Ecol Prog Ser 51:201–213CrossRefGoogle Scholar
  60. Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Fisheries Research Board of Canada, Minister of Supply and Service Canada, OttawaGoogle Scholar
  61. Strickland JDH, Parsons TR (1977) A practical handbook of seawater analysis. Fisheries Research Board of Canada, Minister of Supply and Service Canada, OttawaGoogle Scholar
  62. Suttle CA, Chan AM, Cottrell MT (1990) Infection of phytoplankton by viruses and reduction of primary productivity. Nature 347:467–469CrossRefGoogle Scholar
  63. Suttle CA, Chan AM, Fuhrman JA (1991) Dissolved free amino acids in the Sargasso Sea: uptake and respiration rates, turnover times, and concentrations. Mar Ecol Prog Ser 70:189–199CrossRefGoogle Scholar
  64. Suzuki MT, Taylor LT, Delong EF (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5′-nuclease assays. Appl Environ Microbiol 66:1167–1179CrossRefGoogle Scholar
  65. Tabor CW, Tabor H (1966) Transport systems for 1,4-diaminobutane, spermidine, and spermine in Escherichia coli. J Biol Chem 241:3714–3723Google Scholar
  66. Tabor CW, Tabor H (1985) Polyamines in microorganisms. Microbiol Rev 49:81–99Google Scholar
  67. Tabor H, Rosenthal SM, Tabor CW (1958) The biosynthesis of spermidine and spermine from putrescine and methionine. J Biol Chem 233:907–914Google Scholar
  68. ter Braak CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for Canonical Community Ordination (version 4.5). Microcomputer Power, IthacaGoogle Scholar
  69. Tolar BB, King GM, Hollibaugh JT (2013) An analysis of Thaumarchaeota populations from the northern Gulf of Mexico. Front Microbiol 4(72):1–36Google Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Qian Liu
    • 1
  • Xinxin Lu
    • 2
  • Bradley B. Tolar
    • 1
  • Xiaozhen Mou
    • 2
  • James T. Hollibaugh
    • 1
  1. 1.Department of Marine SciencesUniversity of GeorgiaAthensUSA
  2. 2.Department of Biological SciencesKent State UniversityKentUSA

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