Effects of iron limitation on growth and carbon metabolism in oceanic and coastal heterotrophic bacteria

Limnology and Oceanography

Volumn 59, Issue 2, 2014, Pages 349-360

  Fourquez, Marion ^a,b,e   Devez, Aurélie ^a,b   Schaumann, Annick ^b,c,d   Guéneuguès, Audrey ^a,b   Jouenne, Thierry ^b,c,d   Obernosterer, Ingrid ^a,b   Blain, Stéphane ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

^c NORMANDIE UNIVERSITÉ   (France)

^d Plateforme Instrumentale en Sciences Séparatives et Analytiques de Rouen Institut de Recherche de l'Innovation Biomédicale   (France)

^e UNIVERSITY OF TASMANIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; BIOGEOCHEMICAL CYCLE; ENZYME ACTIVITY; GROWTH RATE; HETEROTROPHY; IRON; MARINE ECOSYSTEM; METABOLISM; NUTRIENT LIMITATION; PROTEOMICS; RESPIRATION;

EID: 84895897569     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2014.59.2.0349     Document Type: Article

References (61)

1. ANDREWS, S. C., A. K. ROBINSON, AND F. RODRÍGUEZ-QUIÑONES. 2003. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27: 215-237, doi:10.1016/S0168-6445(03)00055-X
2. ARMSTRONG, E., J. GRANGER, E. L. MANN, AND N. M. PRICE. 2004. Outer-membrane siderophore receptors of heterotrophic oceanic bacteria. Limnol. Oceanogr. 49: 579-587, doi:10.4319/lo.2004.49.2.0579
3. BAUMANN, L., P. BAUMANN, M. MANDEL, AND R. D. ALLEN. 1972. Taxonomy of aerobic marine eubacteria. J. Bacteriol. 110: 402-429.
4. BEINERT, H., R. H. HOLM, AND E. MÜNCK. 1997. Iron-sulfur clusters: Nature's modular, multipurpose structures. Science. 277: 653-659, doi:10.1126/science.277.5326.653
5. BERMAN-FRANK, I., J. T. CULLEN, Y. SHAKED, R. M. SHERRELL, G. RAM, AND P. G. FALKOWSKI. 2010. Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium. Limnol. Oceanogr. 46: 1249-1260, doi:10.4319/lo.2001.46.6.1249
6. 12 nutrition. Front. Microbiol. 2: 160, doi:10.3389/fmicb.2011.00160
7. BLAIN, S., S. BONNET, C. GUIEU, AND C. DE LUMINY. 2008. Dissolved iron distribution in the tropical and subtropical South Eastern Pacific. Biogeosciences 5: 269-280, doi:10.5194/bg-5-269-2008
8. BONNET, S., AND C. GUIEU. 2006. Atmospheric forcing on the annual iron cycle in the western Mediterranean Sea: A 1-year survey. J. Geophys. Res. 111: C09010, doi:10.1029/ 2005JC003213
9. BOYD, P. W., AND M. J. ELLWOOD. 2010. The biogeochemical cycle of iron in the ocean. Nat. Geosci. 3: 675-682, doi:10.1038/ ngeo964
10. BUCCIARELLI, E., P. PONDAVEN, AND G. SARTHOU. 2010. Effects of an iron-light co-limitation on the elemental composition (Si, C, N) of the marine diatoms Thalassiosira oceanica and Ditylum brightwellii. Biogeosciences 7: 657-669, doi:10.5194/ bg-7-657-2010
11. CHURCH, M. J., D. A. HUTCHINS, AND H. W. DUCKLOW. 2000. Limitation of bacterial growth by dissolved organic matter and iron in the Southern Ocean. Appl. Environ. Microbiol. 66: 455-466, doi:10.1128/AEM.66.2.455-466.2000
12. COTTRELL, M. T., AND D. L. KIRCHMAN. 2003. Contribution of major bacterial groups to bacterial biomass production (thymidine and leucine incorporation) in the Delaware estuary. Limnol. Oceanogr. 48: 168-178, doi:10.4319/ lo.2003.48.1.0168
13. DEL GIORGIO, P. A., AND J. J. COLE. 1998. Bacterial growth efficiency in natural aquatic systems. Annu. Rev. Ecol. Syst. 29: 503-541, doi:10.1146/annurev.ecolsys.29.1.503
14. FAGERBAKKE, K. M., M. HELDAL, AND S. NORLAND. 1996. Content of carbon, nitrogen, oxygen, sulfur and phosphorus in native aquatic and cultured bacteria. Aquat. Microb. Ecol. 10: 15-27, doi:10.3354/ame010015
15. FLINT, D. H., M. H. EMPTAGE, AND J. R. GUEST. 1992. Fumarase A from Escherichia coli: Purification and characterization as an iron-sulfur cluster containing enzyme. Biochemistry 31: 10331-10337, doi:10.1021/bi00157a022
16. 55Fe for microautoradiography and CARD-FISH of natural bacterial communities. FEMS Microbiol. Lett. 337: 132-139, doi:10.1111/1574-6968.12022
17. GARCÍA-MARTÍNEZ, J., S. G. ACINAS, R. MASSANA, AND F. RODRÍGUEZ-VALERA. 2002. Prevalence and microdiversity of Alteromonas macleodii-like microorganisms in different oceanic regions. Environ. Microbiol. 4: 42-50, doi:10.1046/ j.1462-2920.2002.00255.x
18. GRANGER, J., AND N. M. PRICE. 1999. The importance of siderophores in iron nutrition of heterotrophic marine bacteria. Limnol. Oceanogr. 44: 541-555, doi:10.4319/ lo.1999.44.3.0541
19. HEISSENBERGER, A., G. G. LEPPARD, AND G. J. HERNDL. 1996. Relationship between the intracellular integrity and the morphology of the capsular envelope in attached and freeliving marine bacteria. Appl. Environ. Microbiol. 62: 4521-4528.
20. HOPKINSON, B. M., AND K. A. BARBEAU. 2011. Iron transporters in marine prokaryotic genomes and metagenomes. Environ. Microbiol. 14: 114-128, doi:10.1111/j.1462-2920.2011.02539.x
21. HUBBARD, J. A. M., K. B. LEWANDOWSKA, M. N. HUGHES, AND R. K. POOLE. 1986. Effects of iron-limitation of Escherichia coli on growth, the respiratory chains and gallium uptake. Arch. Microbiol. 146: 80-86, doi:10.1007/BF00690163
22. HUBMACHER, D., B. F. MATZANKE, AND S. ANEMÜLLER. 2003. Effects of iron limitation on the respiratory chain and the membrane cytochrome pattern of the euryarchaeon Halobacterium salinarum. Biol. Chem. 384: 1565-1573, doi:10.1515/ BC.2003.173
23. HUDSON, R. J. M., AND F. M. M. MOREL. 1989. Distinguishing between extra-and intracellular iron in marine phytoplankton. Limnol. Oceanogr. 34: 1113-1120, doi:10.4319/ lo.1989.34.6.1113
24. IVARS-MARTÍNEZ, E., G. D'AURIA, F. RODRÍGUEZ-VALERA, C. SÁNCHEZ-PORRO, A. VENTOSA, I. JOINT, AND M. MÜHLING. 2008a. Biogeography of the ubiquitous marine bacterium Alteromonas macleodii determined by multilocus sequence analysis. Mol. Ecol. 17: 4092-4106, doi:10.1111/j.1365-294X.2008.03883.x
25. IVARS-MARTÍNEZ, E., AND OTHERS. 2008b. Comparative genomics of two ecotypes of the marine planktonic copiotroph Alteromonas macleodii suggests alternative lifestyles associated with different kinds of particulate organic matter. ISME J. 2: 1194-1212, doi:10.1038/ismej.2008.74
26. KAPLAN, J., D. MCVEY WARD, R. J. CRISP, AND C. C. PHILPOTT. 2006. Iron-dependent metabolic remodeling in S. cerevisiae. Biochim. Biophys. Acta 1763: 646-651, doi:10.1016/ j.bbamcr.2006.03.008
27. KENNEDY, M. C., M. H. EMPTAGE, J. L. DREYER, AND H. BEINERT. 1983. The role of iron in the activation-inactivation of aconitase. J. Biol. Chem. 258: 11098-11105.
28. KIRCHMAN, D. L., K. A. HOFFMAN, R. WEAVER, AND D. A. HUTCHINS. 2003. Regulation of growth and energetics of a marine bacterium by nitrogen source and iron availability. Mar. Ecol. Prog. Ser. 250: 291-296, doi:10.3354/meps250291
29. KIRCHMAN, D. L., R. G. KEIL, AND P. A. WHEELER. 1990. Carbon limitation of ammonium uptake by heterotrophic bacteria in the subarctic Pacific. Limnol. Oceanogr. 35: 1258-1266, doi:10.4319/lo.1990.35.6.1258
30. LAPORTE, D. C. 1993. The isocitrate dehydrogenase phosphorylation cycle: Regulation and enzymology. J. Cell. Biochem. 51: 14-18, doi:10.1002/jcb.240510104
31. LOMMER, M., AND OTHERS. 2012. Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation. Genome Biol. 13: R66, doi:10.1186/gb-2012-13-7-r66
32. MALDONADO, M. T., AND N. M. PRICE. 1999. Utilization of iron bound to strong organic ligands by plankton communities in the subarctic Pacific Ocean. Deep-Sea Res. II 46: 2447-2473, doi:10.1016/S0967-0645(99)00071-5
33. MARCHETTI, A., AND OTHERS. 2009. Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature 457: 467-470, doi:10.1038/nature07539
34. MARIE, D., F. PARTENSKY, S. JACQUET, AND D. VAULOT. 1997. Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl. Environ. Microbiol. 63: 186-193.
35. MILLERO, F. J., S. SOTOLONGO, AND M. IZAGUIRRE. 1989. The oxidation kinetics of Fe(II) in seawater. Geochim. Cosmochim. Acta 51: 793-801, doi:10.1016/0016-7037(87)90093-7
36. MIONI, C. E., S. M. HANDY, M. J. ELLWOOD, M. R. TWISS, R. M. L. MCKAY, P. W. BOYD, AND S. W. WILHELM. 2005. Tracking changes in bioavailable Fe within high-nitrate low-chlorophyll oceanic waters: A first estimate using a heterotrophic bacterial bioreporter. Global Biogeochem. Cycles 19: 1-10, doi:10.1029/2005GB002476
37. MOREL, F. M. M., AND J. G. RUETER. 1979. Aquil: A chemically defined phytoplankton culture medium for trace metal studies. J. Phycol. 15: 135-141, doi:10.1111/j.0022-3646.1979.00135.x
38. MORRISSEY, J., AND C. BOWLER. 2012. Iron utilization in marine cyanobacteria and eukaryotic algae. Front. Microbiol. 3: 1-13, doi:10.3389/fmicb.2012.00043
39. OBERNOSTERER, I., R. LAMI, M. LARCHER, N. BATAILLER, P. CATALA, AND P. LEBARON. 2010. Linkage between bacterial carbon processing and the structure of the active bacterial community at a coastal site in the NW Mediterranean Sea. Microb. Ecol. 59: 428-435, doi:10.1007/s00248-009-9588-7
40. OEXLE, H., E. GNAIGER, AND G. WEISS. 1999. Iron-dependent changes in cellular energy metabolism: Influence on citric acid cycle and oxidative phosphorylation. Biochim. Biophys. Acta 1413: 99-107, doi:10.1016/S0005-2728(99)00088-2
41. PAKULSKI, J. D., AND OTHERS. 1996. Iron stimulation of Antarctic bacteria. Nature 383: 133-134, doi:10.1038/383133b0
42. PARENTE, A. F. A., A. M. BAILÃO, C. L. BORGES, J. A. PARENTE, A. D. MAGALHÃES, C. A. O. RICART, AND C. M. A. SOARES. 2011. Proteomic analysis reveals that iron availability alters the metabolic status of the pathogenic fungus Paracoccidioides brasiliensis. PLoS One 6: 1-14, doi:10.1371/journal.pone. 0022810
43. PHILPOTT, C. C., S. LEIDGENS, AND A. G. FREY. 2012. Metabolic remodeling in iron-deficient fungi. Biochim. Biophys. Acta 1823: 1509-1520, doi:10.1016/j.bbamcr.2012.01.012
44. PRICE, N. M., G. I. HARRISON, J. G. HERING, R. J. HUDSON, P. M. V. NIREL, B. PALENIK, AND F. M. M. MOREL. 1989. Preparation and chemistry of the artificial algal culture medium Aquil. Biol. Oceanogr. 6: 443-461.
45. PUKALL, R., AND OTHERS. 1999. High sequence diversity of Alteromonas macleodii-related cloned and cellular 16S rDNAs from a Mediterranean seawater mesocosm experiment. FEMS Microbiol. Ecol. 28: 335-344, doi:10.1111/j.1574-6941.1999. tb00588.x
46. RICHARDSON, D. J. 2000. Bacterial respiration: A flexible process for a changing environment. Microbiology 146: 551-571.
47. RUSSELL, J. B., AND G. M. COOK. 1995. Energetics of bacterial growth: Balance of anabolic and catabolic reactions. Microbiol. Rev. 59: 48-62.
48. SAITO, M. A., AND OTHERS. 2011. Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii. Proc. Natl. Acad. Sci. U. S. A. 108: 2184-2189, doi:10.1073/pnas.1006943108
49. SINGER, T. P., AND M. K. JOHNSON. 1985. The prosthetic groups of succinate dehydrogenase: 30 years from discovery to identification. FEBS Lett. 190: 189-198, doi:10.1016/0014-5793(85)81282-5
50. SMITH, D. P., AND OTHERS. 2010. Transcriptional and translational regulatory responses to iron limitation in the globally distributed marine bacterium Candidatus pelagibacter ubique. PLoS One 5: e10487, doi:10.1371/journal.pone.0010487
51. STRZEPEK, R. F., AND P. J. HARRISON. 2004. Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 403: 689-692, doi:10.1038/nature02954
52. STRZEPEK, R. F., M. T. MALDONADO, K. A. HUNTER, R. D. FREW, AND P. W. BOYD. 2011. Adaptive strategies by Southern Ocean phytoplankton to lessen iron limitation: Uptake of organically complexed iron and reduced cellular iron requirements. Limnol. Oceanogr. 56: 1983-2002, doi:10.4319/lo.2011. 56.6.1983
53. SULAEMAN, S., M. HERNOULD, A. SCHAUMANN, L. COQUET, J.-M. BOLLA, E. DÉ, AND O. TRESSE. 2012. Enhanced adhesion of Campylobacter jejuni to abiotic surfaces is mediated by membrane proteins in oxygen-enriched conditions. PLoS One 7: e46402, doi:10.1371/journal.pone.0046402
54. SUNDA, W., AND S. HUNTSMAN. 2003. Effect of pH, light, and temperature on Fe-EDTA chelation and Fe hydrolysis in seawater. Mar. Chem. 84: 35-47, doi:10.1016/S0304-4203 (03)00101-4
55. SUNDA, W. G., AND S. A. HUNTSMAN. 1995. Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar. Chem. 50: 189-206, doi:10.1016/0304-4203(95)00035-P
56. SUNDA, W. G., N. M. PRICE, AND F. M. M. MOREL. 2005. Trace metal ion buffers and their use in culture studies, p. 35-63. In R. Anderson [ed.], Algal culturing techniques. Academic Press.
57. THIERY, P. 1967. Technique acide périodique thiosemicarbazideprotéinate d'argent. J. Microsc. 6: 987-1018. [Periodic acidthiosemicarbazide-silver proteinate technique.]
58. TORTELL, P. D., M. T. MALDONADO, J. GRANGER, AND N. M. PRICE. 1999. Marine bacteria and biogeochemical cycling of iron in the oceans. FEMS Microbiol. Ecol. 29: 1-11, doi:10.1111/j.1574-6941.1999.tb00593.x
59. TORTELL, P. D., M. T. MALDONADO, J. GRANGER, AND N. M. PRICE. 1996. The role of heterotrophic bacteria in iron-limited ocean ecosystems. Nature 383: 330-332, doi:10.1038/383330a0
60. WONG, D. K., B.-Y. LEE, M. A. HORWITZ, AND W. GIBSON. 1999. Identification of Fur, aconitase, and other proteins expressed by Mycobacterium tuberculosis under conditions of low and high concentrations of iron by combined two-dimensional gel electrophoresis and mass spectrometry. Infect. Immun. 67: 327-336.
61. YOOSEPH, S., AND OTHERS. 2010. Genomic and functional adaptation in surface ocean planktonic prokaryotes. Nature 468: 60-66, doi:10.1038/nature09530