Distribution of heterotrophic bacteria and virus-like particles along a salinity gradient in a hypersaline coastal lagoon

Aquatic Microbial Ecology

Volumn 54, Issue 2, 2009, Pages 171-183

  Schapira, Mathilde ^a,b   Buscot, Marie Jeanne ^a   Leterme, Sophie C ^a,c   Pollet, Thomas ^d   Chapperon, Coraline ^a   Seuront, Laurent ^a,c  

^a FLINDERS UNIVERSITY   (Australia)

^b RHODES UNIVERSITY   (South Africa)

^c SOUTH AUSTRALIAN RESEARCH AND DEVELOPMENT INSTITUTE   (Australia)

^d UNIVERSITÉ DE SAVOIE   (France)

Author keywords

Heterotrophic bacteria; Hypersaline lagoon; Salinity; Virus like particles

Indexed keywords

BACTERIA (MICROORGANISMS); PROKARYOTA;

EID: 61949199663     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame01262     Document Type: Article

References (75)

1. Ayadi H, Abid O, Elloumi J, Bouaïn A, Sime-Ngando T (2004) Structure of the phytoplankton communities in two lagoons of different salinity in the Sfax saltern (Tunisia). J Plankton Res 26:669-679
2. Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nature 5:782-791
3. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad TF (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257-263
4. Benlloch S, Lopez-Lopez A, Casamayor EO, Smerdon G and others (2002) Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ Microbiol 4:349-360
5. Benner R, Opsahl S (2001) Molecular indicators of the sources and transformations of dissolved organic matter in the Mississippi river plume. Org Geochem 32:597-611
6. Bouvier TC, del Giorgio PA (2002) Compositional changes in free-living bacteria communities along a salinity gradient in two temperate estuaries. Limnol Oceanogr 47:453-470
7. Bouvier TC, del Giorgio PA, Gasol JM (2007) A comparative study of the cytometric characteristics of high and low nucleic-acid bacterioplankton cells from different aquatic ecosystems. Environ Microbiol 9:2050-2066
8. Brussaard CPD (2004) Optimization of procedures for counting viruses by flow cytometry. Appl Environ Microbiol 70:1506-1513
9. Brussaard CPD, Thyrhaug R, Marie D, Bratbak G (1999) Flow cytometric analysis of viral infection in two marine phytoplankton species, Micromonas pusilla (Prasinophyceae) and Phaeocystis pouchetii (Prymnesiophyceae). J Phycol 35:941-948
10. Brussaard CPD, Kuipers B, Veldhuis MJW (2005) A mesocosm study of Phaeocystis globosa population dynamics. I. Regulatory role of viruses in bloom control. Harmful Algae 4:859-874
11. Brussaard CPD, Timmermans KR, Uitz J, Veldhuis MJW (2008) Virioplankton dynamics and virally induced phytoplankton lysis versus microzooplankton grazing southeast of the Kerguelen (Southern Ocean). Deep-Sea Res II 55:752-765
12. Choi DH, Cho BC (2005) Idiomarina seosinensis sp. nov., isolated from hypersaline water of a solar saltern in Korea. Int J Syst Evol Microbiol 55:379-383
13. Clarke KR, Warwick RM (1994) Similarity-based testing for community pattern: the 2-way layout with no replication. Mar Biol 118:167-176
14. Clarke KR, Warwick RM (2001) A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Mar Ecol Prog Ser 216:265-278
15. Crump BC, Hopkinson CS, Sogin ML, Hobbie JE (2004) Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Appl Environ Microbiol 70:1494-1505
16. Cunha MA, Almeida MA, Alcantara F (2000) Patterns of ectoenzymatic and heterotrophic bacterial activities along a salinity gradient in a shallow tidal estuary. Mar Ecol Prog Ser 204:1-12
17. Dauvin JC, Bachelet G, Bellan G (2006) Biodiversity and biogeographic relationships of the polychaete fauna in French Atlantic and Mediterranean waters. Sci Mar 70:259-267
18. del Giorgio PA, Bouvier TC (2002) Linking the physiologic and phylogenetic successions in free-living bacterial communities along an estuarine salinity gradient. Limnol Oceanogr 47:471-486
19. del Giorgio PA, Scarborough G (1995) Increase in the proportion of metabolically active bacteria along gradients of enrichment in freshwater and marine plankton: implications for estimates of bacterial growth and production rates. J Plankton Res 17:1905-1924
20. del Giorgio PA, Prairie YT, Bird DE (1997) Coupling between rates of bacterial production and the abundance of metabolically active bacteria in lakes, counted using CTC reduction and flow cytometry. Microb Ecol 34:144-154
21. Demergasso C, Casamayor EO, Chong G, Galleguillos P, Escudero L, Pédros-Alió C (2004) Distribution of prokaryotic genetic diversity in athalassohaline lakes of the Atacama Desert, Northern Chile. FEMS Microbiol Ecol 48:57-69
22. Demergasso C, Escudero L, Casamayor EO, Chong G, Balagué V, Pedros-Alio C (2008) Novelty and spatio-temporal heterogeneity in the bacterial diversity of hypersaline Lake Tebenquiche (Salar de Atacama). Extremophiles 12:491-504
23. Diez B, Anton J, Guixa-Boixareu N, Pédros-Alió C, Rodriguez-Valera F (2000) Pulsed-field gel electrophoresis analysis of virus assemblages present in a hypersaline environment. Int Microbiol 3:159-164
24. Fofonoff N, Millard RC (1983) Algorithms for computation of fundamental properties of seawater. UNESCO Tech Pap Mar Sci no. 44. UNESCO, Paris
25. Ford PW (2007) Biogeochemistry of the Coorong: review and identification of future research requirements. Water for a Healthy Country Flagship. CSIRO, Canberra
26. Forsgren G, Jansson M, Nilsson P (1996) Aggregation and sedimentation of iron, phosphorus and organic carbon in experimental mixtures of freshwater and estuarine waters. Estuar Coast Shelf Sci 43:259-268
27. Foti MJ, Sorokin DY, Zacharova EE, Pimenov NV, Kuenen JG, Muyzer G (2008) Bacterial diversity and activity along a salinity gradient in soda lakes of the Kulunda Steppe (Altai, Russia). Extremophiles 12:133-145
28. Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399:541-548
29. Gasol JM, del Giorgio PA (2000) Using flow cytometry for counting natural plankton bacteria and understanding the structure of planktonic bacterial community. Sci Mar 64:197-224
30. Gasol JM, Zweifel UL, Peters F, Fuhrman JA, Hagstrom A (1999) Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria. Appl Environ Microbiol 65:4475-4483
31. Geddes M (2005) Ecological outcomes from the small barrage outflow of August 2004. Final report prepared for the Department of Water, Land and Biodiversity Conservation. SARDI Research Report Series no. 116. SARDI Aquatic Sciences, Adelaide
32. Guixa-Boixareu N, Calderón-Paz J, Heldal M, Bratbak G, Pedrós-Alió C (1996) Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient. Aquat Microb Ecol 11:215-227
33. Hedges JI, Keil RG (1999) Organic geochemical perspectives on estuarine processes: sorption reactions and consequences. Mar Chem 65:55-65
34. Hewson I, O'Neil JM, Fuhrman JA, Dennison WC (2001) Virus-like particles distribution and abundances in sediments and overlaying waters along eutrophication gradients in two subtropical estuaries. Limnol Oceanogr 46:1734-1746
35. Humayoun SB, Bano N, Hollibaugh JT (2003) Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Appl Environ Microbiol 69: 1030-1042
36. Javor BJ (1989) Hypersaline environment: microbiology and biocheochemistry. Springer-Verlag, New York
37. Jiang H, Dong H, Zhang G, Yu B, Chapman LR, Fields MW (2006) Microbial diversity in water and sediment of Lake Chaka, a athalassohaline lake in Northwestern China. Appl Environ Microbiol 72:3832-3845
38. Jiang SC, Paul JH (1994) Seasonal and diel abundances of viruses and occurrence of lysogeny/bacteriocinogeny in the marine environment. Mar Ecol Prog Ser 104:163-172
39. Jochem FJ, Lavrentyev PJ, First MR (2004) Growth and grazing rates of bacteria groups with different apparent DNA content in the Gulf of Mexico. Mar Biol 145:1213-1225
40. Joint I, Henriksen P, Garde K, Riemann B (2002) Primary production, nutrient assimilation and microzooplankton grazing along a hypersaline gradient. FEMS Microbiol Ecol 39:245-257
41. Kaiser MJ, Attril MJ, Jennings S, Thomas DN and others (2005) Estuarine ecology. In: Kaiser MJ (ed) Marine ecology: processes, systems, and impacts. Oxford University Press, New York
42. Kan J, Crump BC, Wang K, Chen F (2006) Bacterioplankton community in Chesapeake Bay: predictable or random assemblages. Limnol Oceanogr 51:2157-2169
43. Langenheder S, Kisand V, Wikner J, Tranvik L (2003) Salinity as a structuring factor for the composition and performance of bacterioplankton degrading riverine DOC. FEMS Microbiol Ecol 45:189-202
44. Laybourn-Parry J, Marshall WA, Madan NJ (2007) Viral dynamics and patterns of lysogeny in saline Antarctic lakes. Polar Biol 30:351-358
45. Lebaron P, Servais P, Baudoux AC, Bourrain M, Courties C, Parthuisot N (2002) Variation of bacterial-specific activity with cell size and nucleic acid content assessed by flow cytometry. Aquat Microb Ecol 28:131-140
46. Legendre P, Legendre L (2003) Numerical ecology. In: Legendre P, Legendre L (eds) Developments in environmental modelling. Elsevier Science, Amsterdam, p 33-47
47. Lenski RE (1988) Dynamics of interactions between bacteria and virulent bacteriophages. Adv Microb Ecol 10:1-44
48. Li WKW, Jellett JF, Dickie PM (1995) DNA distributions in planktonic bacteria stained with TOTO or TO-PRO. Limnol Oceanogr 40:1485-1495
49. Longnecker K, Sherr BF, Sherr EB (2005) Activity and phylogenetic diversity of bacterial cells with high and low nucleic acid content and electron transport system activity in an upwelling ecosystem. Appl Environ Microbiol 71:7737-7749
50. Lymer D, Vrede K (2006) Nutrient additions resulting in phage release and formation of non-nucleoid-containing bacteria. Aquat Microb Ecol 43:107-112
51. Madan N, MarshallWA, Laybourn-Parry J (2005) Viruses and microbial loop dynamics over an annual cycle in three contrasting Antarctic lakes. Freshw Biol 50:1291-1300
52. Marchant H, Davidson A, Wright S, Glazebrook J (2000) The distribution and abundance of viruses in the Southern Ocean during spring. Antarct Sci 12:414-417
53. Marie D, Partensky F, Jacquet S, Vaulot D (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
54. Marie D, Brussaard CPD, Thyrhaug R, Bratbak G, Vaulot D (1999a) Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl Environ Microbiol 65:45-52
55. Marie D, Partensky F, Vaulot D, Brussaard CPD (1999b) Numeration of phytoplankton, bacteria and viruses in marine samples. In: Robingson JP, Darzynkiewicz Z, Dean PN, Orfao A, Rabinovitch P, Stewart CC, Tanke HJ, Wheless LL (eds) Current protocols in cytometry, Suppl 10, Unit 11.11. John Wiley & Sons, New York, p 1-15
56. Noble RT, Fuhrman JA (1998) Use of the SYBR Green 1 for rapid fluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14:113-118
57. Oren A (1999) The enigma of square and triangular halophilic Archaea. In: Seckbach J (ed) Enigmatic microorganisms and life in extreme environments. Kluwer, Dordrecht, p 337-355
58. Park JS, Kim HJ, Choi DH, Cho BC (2003) Active flagellates grazing on prokaryotes in high salinity waters of a solar saltern. Aquat Microb Ecol 33:173-179
59. Pedrós-Alió C, Calderón JC, Gasol JM (2000a) Comparative analysis shows that bacterivory, not viral lysis, controls the abundance of heterotrophic prokaryotic plankton. FEMS Microbiol Ecol 32:157-165
60. Pedrós-Alió C, Calderón-Paz J, MacLean MH, Medina G, Marrasé C, Gasol JM, Guixa-Boixareu N (2000b) The microbial food web along salinity gradient. FEMS Microbiol Ecol 32:143-155
61. Rodriguez-Valera F (1988) Characteristics and microbial ecology of hypersaline environments. In: Rodriguez-Valera F (ed) Halophilic bacteria, Vol. 1. CRC Press, Boca Raton, FL
62. Rodriguez-Valera F (1993) Introduction to saline environments. In: Vreeland R, Hochstein LI (eds) The biology of halophilic bacteria. CRC Press, Boca Raton, FL, p 1-24
63. Sandaa RA, Skjoldal EF, Bratbak G (2003) Virioplankton community structure along a salinity gradient in a solar saltern. Extremophiles 7:347-351
64. Santos F, Meyerdierks A, Pena A, Rossello-Mora R, Amman R, Anton J (2007) Metagenomic approach to the study of halophages: the environmental halophage 1. Environ Microbiol 9:1711-1723
65. Servais P, Casamayor EO, Courties C, Catala P, Parthuisot N, Lebaron P (2003) Activity and diversity of bacterial cells with high and low nucleic acid content. Aquat Microb Ecol 33:41-51
66. Seymour JR, Mitchell JG, Seuront L (2004) Microscale heterogeneity in the activity of coastal bacterioplankton communities. Aquat Microb Ecol 35:1-16
67. Seymour JR, Seuront L, Mitchell JG (2005) Microscale and small-scale temporal dynamics of a coastal planktonic microbial community. Mar Ecol Prog Ser 300:21-37
68. Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Bull Fish Res Board Can 167:1-311
69. Suttle CA (2007) Marine viruses: major players in the global ecosystem. Nature 5:801-812
70. Webster W, Ford P, Lamontagne S, Leaney I (2004) Environmental flow requirements for the Coorong, Lower Lakes and Murray Mouth. Water for Healthy Country National Research Flagship. CSIRO Land and Water, Canberra
71. Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127-181
72. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69-114
73. Wu QL, Zwart G, Schauer M, Kamst-van Agterveld MP, Hahn MW (2006) Bacterioplankton community composition along a salinity gradient of sixteen high-mountain lakes located on the Tibetan Plateau, China. Appl Environ Microbiol 72:5478-5485
74. Zar JH (1996) Biostatistical analysis. Prentice Hall, Upper Saddle River, NJ
75. Zubkov MV, Fuchs BM, Burkill PH, Amann R (2001) Comparison of cellular and biomass specific activities of dominant bacterioplankton groups in stratified waters of the Celtic Sea. Appl Environ Microbiol 67:5210-5218