The Relationship between Salinity and Bacterioplankton in Three Relic Coastal Ponds (Macchiatonda Wetland, Italy)

Matteo Evangelisti, Domenico D’Amelia, Gustavo Di Lallo, Maria Cristina Thaller, Luciana Migliore

Department of Biology, Tor Vergata University, Rome, Italy.
Riserva Naturale Regionale Macchiatonda, Rome, Italy.

DOI: 10.4236/jwarp.2013.59087                

Abstract

The great environmental importance of wetlands is linked to the high biodiversity of flora and fauna they support, so that the international Ramsar Convention focused on these areas and highlighted the need to preserve them. The bacterial communities that thrive in these ecosystems play a key role in regulating the local biogeochemical processes and yet their distribution, abundance and dynamics are poorly known. This work is aimed to study the bacterial assemblages over a year long, to contribute to the understanding of the natural processes occurring in wetlands at variable salinity. The knowledge of bacterial groups, species or assemblages can provide a useful bioindicator for conservation and restoration efforts. Macchiatonda Natural Reserve (Santa Severa, Rome, Italy) is a relic ecosystem, once found along the entire Tyrrhenian coast. This wetland encompasses three coastal ponds with different salinity, where both peculiar vegetation and highly diverse migratory and resident avifauna can be found. This ancient system has been scarcely investigated and nothing is known about its microbial community. The molecular metagenomic analyses performed to investigate the salinity/bacterioplankton relationship, highlighted differences in the bacterial structure, between ponds and seasons. Analogous trends in SSCP profiles, Shannon Index, and bacterial composition (16S) were observed in the two saltier ponds, whereas the entire set of results was different for the less salty one. The species diversity in the three ponds varied according the salinity gradient, with the maximum diversity corresponding to a salt concentration range between 20 and 30. At higher and lower salinity, the microbial diversity lowers, according to the “Intermediate Disturbance Hypothesis”.

Keywords

Bacterioplankton; Coastal Ponds; Diversity; Salinity; SSCP; Wetlands

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	A. M. Anderson, D. A. Haukos and J. T. Anderson, “Habitat Use by Anurans Emerging and Breeding in Playa Wetlands,” Wildlife Society Bulletin, Vol. 27, No. 3, 1999, pp. 759-769.
[2]	K. R. Russell, D. C. Guynnand Jr. and H. G. Hanlin, “Importance of Small Isolated Wetlands for Herpetofaunal Diversity in Managed, Young Growth Forests in the Coastal Plain of South Carolina,” Forest Ecology and Management, Vol. 163, No. 1-3, 2002, pp. 43-59. doi:10.1016/S0378-1127(01)00526-6
[3]	R. W. Nairn and W. J. Mitsch, “Phosphorus Removal in Created Wetland Ponds Receiving River Overflow,” Ecological Engineering, Vol. 14, No. 1-2, 1999, pp. 107-126. doi:10.1016/S0378-1127(01)00526-6
[4]	N. Wang and W. J. Mitsch, “Detailed Ecosystem Model of Phosphorus Dynamics in Created Riparian Wetlands,” Ecological Modelling, Vol. 126, No. 2-3, 2000, pp. 101-130. doi:10.1016/S0304-3800(00)00260-X
[5]	W. J. Mitsch, J. W. Day, L. Zhang and R. R. Lane, “Nitrate-Nitrogen Retention in Wetlands in the Mississippi River Basin,” Ecological Engineering, Vol. 24, No. 4, 2005, pp. 267-278. doi:10.1016/j.ecoleng.2005.02.005
[6]	M. M. Brinson, A. E. Lugo and S. Brown, “Primary Productivity, Decomposition and Consumer Activity in Freshwater Wetlands,” Annual Review of Ecology and Systematics, Vol. 12, No. 1, 1981, pp. 123-161. doi:10.1146/annurev.es.12.110181.001011
[7]	R. G. Wetzel, “Wetlands as Metabolic Gates,” Journal of Great Lakes Research, Vol. 18, No. 4, 1992, pp. 529-532. doi:10.1016/S0380-1330(92)71320-3
[8]	J. Wang, D. Yang, Y. Zhang, J. Shen, C. van der Gast, M. W. Hahn and Q. Wu, “Do Patterns of Bacterial Diversity along Salinity Gradients Differ from Those Observed for Macroorganisms?” PlosOne, Vol. 6, No. 11, 2011, pp. 1-8.
[9]	J. V. McArthur, “Bacteria as Biomonitors,” In: R. B. Rader, D. P. Batzer and S. A. Wissinger, Eds., Bioassessment and Management of North American Freshwater Wetlands, John Wiley & Sons, New York, 2001, pp. 249-261.
[10]	M. Merkley, B. R. Russell, J. V. McArthur and D. Eggett, “Bacteria as Bioindicators in Wetlands: Bioassessment in the Bonneville Basin of Utah, USA,” Wetlands, Vol. 24, No. 3, 2004, pp. 600-607. doi:10.1672/0277-5212(2004)024[0600:BABIWB]2.0.CO;2
[11]	ISPRA, “Repertorio Nazionale Interventi di Ripristino, 3b Lazio ‘Ricostruzione Dell’ Ecosistema Dunale di Macchiatonda,” 2008.
[12]	Riserva Naturale di Macchiatonda, “LIFE Project CO.ME.BIS. Relazione Monitoraggio Interventi di Ripristino,” 2009. http://www.lifecomebis.eu/comebis.cfm
[13]	K. H. Bostrom, K. Simu, A. Hagstrom and R. Lasse, “Optimization of DNA Extraction for Quantitative Marine Bacterioplankton Community Analysis,” Limnology and Oceanography, Vol. 2, No. 1, 2004, pp. 365-373. doi:10.4319/lom.2004.2.365
[14]	G. M. Rossolini, P. Muscas, A. Chiesurim and G. Satta, “Molecular Cloning and Expression in Escherichia coli of the Salmonella Typhi Gene Cluster Coding for Type 1 Fimbriae,” In: F. Cabello, C. Hormaeche and P. Mastroeni, Eds., The Biology of Salmonella, Nato ASI Series, Plenum Press, New York, 1993, pp. 408-412. doi:10.1007/978-1-4615-2854-8_51
[15]	J. Zhou, M. A. Bruns and J. M. Tiedje, “DNA Recovery from Soils of Diverse Composition,” Applied Environmental Microbiology, Vol. 62, No. 2, 1996, pp. 316-322.
[16]	F. Schwieger and C. C. Tebbe, “A New Approach to Utilize PCR-Single-Strand-Conformation Polymorphism for 16S rRNA Gene-Based Microbial Community Analysis,” Applied and Environmental Microbiology, Vol. 64, No. 12, 1998, pp. 4870-4876.
[17]	A. Schmalenberger, F. Schwieger and C. C. Tebbe, “Effect of Primer Hybridizing to Different Evolutionarily Conserved Regions of the Small-Subunit rRNA Gene in PCR-Based Microbial Community Analysis and Genetic Profiling,” Applied Environmental Microbiology, Vol. 67, No. 8, 2001, pp. 3557-3563. doi:10.1128/AEM.67.8.3557-3563.2001
[18]	Y. L. Tsai and B. H. Olson, “Rapid Method for Separation of Bacterial DNA from Humic Substances in Sediments for Polymerase Chain Reaction,” Applied Environmental Microbiology, Vol. 58, No. 7, 1992, pp. 2292-2295.
[19]	B. J. Bassam, G. Caetano-Anolles and P. M. Gresshoff, “Fast and Sensitive Silver Staining of DNA in Polyacrylamide Gels,” Analytical Biochemistry, Vol. 196, No. 1, 1991, pp. 80-83. doi:10.1016/0003-2697(91)90120-I
[20]	S. F. Altschul, W. Gish, W. Miller, E. W. Myers and D. J. Lipman, “Basic Local Alignment Search Tool,” Journal of Molecular Evolution, Vol. 215, No. 3, 1990 pp. 403-410.
[21]	Ø. Hammer, D. A. T. Harper and P. D. Ryan, “PAST: Paleontological Statistics Software Package for Education and Data Analysis,” Palaeontologia Electronica, Vol. 4, 2001. http://palaeo-electronica.org/2001_1/past/issue1_01.htm
[22]	A. Ramette, “Multivariate Analyses in Microbial Ecology,” FEMS Microbiology Ecology, Vol. 62, No. 2, 2007, pp. 142-160. doi:10.1111/j.1574-6941.2007.00375.x
[23]	T. Brinkhoff, H.-A. Giebel and M. Simon, “Diversity, Ecology, and Genomics of the Roseobacter Clade: A Short overview,” Archives of Microbiology, Vol. 189, No. 6, 2008, pp. 531-539. doi:10.1007/s00203-008-0353-y
[24]	H. Dang, T. Li, M. Chen and G. Huang, “Cross-Ocean Distribution of Rhodobacterales Bacteria as Primary Surface Colonizers in Temperate Coastal Marine Waters,” Applied and Environmental Microbiology, Vol. 74, No. 1, 2008, 52-60. doi:10.1128/AEM.01400-07
[25]	S. Spring, R. Schulze, J. Overmann and K.-H. Schleifer, “Identification and Characterization of Ecologically Significant Prokaryotes in the Sediment of Freshwater Lakes: Molecular and Cultivation Studies,” FEMS Microbiology Reviews, Vol. 24, No. 5, 2000, pp. 573-590. doi:10.1111/j.1574-6976.2000.tb00559.x
[26]	T. C. Bouvier and P. A. Del Giorgio, “Compositional Changes in Free-Living Bacterial Communities along a Salinity Gradient in Two Temperate Estuaries,” Limnology and Oceanography, Vol. 47, No. 2, 2002, pp. 453-470. doi:10.4319/lo.2002.47.2.0453
[27]	G. A. F. Lemes, R. Kersanach, L. da S. Pinto, O. A. Dellagostin, J. S. Yunes and A. Matthiensen, “Biodegradation of Microcystins by Aquatic Burkholderia sp. from a South Brazilian Coastal Lagoon,” Ecotoxicology and Environmental Safety, Vol. 69, No. 3, 2008, pp. 358-365. doi:10.1016/j.ecoenv.2007.03.013
[28]	L. Sun, F. Qiu, X. Zhang, X. D. Xiuzhu, Dong and W. Song, “Endophytic Bacterial Diversity in Rice (Oryza sativa L.) Roots Estimated by 16S rDNA Sequence Analysis,” Microbial Ecology, Vol. 55, No. 3, 2008, pp. 415-424. doi:10.1007/s00248-007-9287-1
[29]	Q. L. Wu, G. Zwart, M. Schauer, P. Miranda, M. P. Kamst-van Agterveld and M. W. Hahn, “Bacterioplankton Community Composition along a Salinity Gradient of Sixteen High-Mountain Lakes Located on the Tibetan Plateau, China,” Applied Environmental Microbiology, Vol. 72, No. 8, 2006, pp. 5478-5485. doi:10.1128/AEM.00767-06
[30]	B. C. Crump, C. S. Hopkinson, M. L. Sogin and J. E. Hobbie, “Microbial Biogeography along an Estuarine Salinity Gradient: Combined Influences of Bacterial Growth and Residence Time,” Applied and Environmental Microbiology, Vol. 70, No. 3, 2004, pp. 1494-1505. doi:10.1128/AEM.70.3.1494-1505.2004
[31]	C. A. Lozupone and R. Knight, “Global Patterns in Bacterial Diversity,” Proceedings of the National Academy of Sciences USA, Vol. 104, No. 27, 2007, pp. 11436-11440. doi:10.1073/pnas.0611525104
[32]	C. R. Jackson and S. C. Vallaire, “Effects of Salinity and Nutrients on Microbial Assemblages in Louisiana Wetland Sediment,” Wetlands, Vol. 29, No. 1, 2009, pp. 277-287. doi:10.1672/08-86.1
[33]	J.-C. Auguet, A. Barberán and E. O. Casamayor, “Global Ecological Patterns in Uncultured Archaea,” The ISME Journal, Vol. 4, No. 2, 2010, pp. 182-190. doi:10.1038/ismej.2009.109
[34]	A. Barberán and E. Casamayor, “Global Phylogenetic Community Structure and β-Diversity Patterns in Surface Bacterioplankton Metacommunities,” Aquatic Microbial Ecology, Vol. 59, No. 1, 2010, pp. 1-10. doi:10.3354/ame01389
[35]	C. M. Jones and S. Hallin, “Ecological and Evolutionary Factors Underlying Global and Local Assembly of Denitrifier Communities,” The ISME Journal, Vol. 4, No. 5, 2010, pp. 633-641. doi:10.1038/ismej.2009.152
[36]	L. Tam, P. G. Kevan and J. T. Trevors, “Viable Bacterial Biomass and Functional Diversity in Fresh and Marine Waters in the Canadian Arctic,” Polar Biology, Vol. 26, No. 5, 2003, pp. 287-294.
[37]	I. Boujelben, M. Gomariz, M. Martinez-Garcia, F. Santos, A. Pena, C. Lopez, J. Antonand and S. Maalej, “Spatial and Seasonal Prokaryotic Community Dynamics in Ponds of Increasing Salinity of Sfax Solar Salternin Tunisia,” Antonie van Leeuwenhoek, Vol. 101, No. 4, 2012, pp. 845-857. doi:10.1007/s10482-012-9701-7
[38]	M. Estrada, P. Henriksen, J. M. Gasol, E. O. Casamayor and C. Pedros-Alio, “Diversity of Planktonic Photoautotrophic Microorganisms along a Salinity Gradient as Depicted by Microscopy, Flow Cytometry, Pigment Analysis and DNA-Based Methods,” FEMS Microbiology Ecology, Vol. 49, No. 2, 2004, pp. 281-293. doi:10.1016/j.femsec.2004.04.002
[39]	M. Schapira, M. J. Buscot, S. C. Leterme, T. Pollet, C. Chapperon and L. Seuront, “Distribution of Heterotrophic Bacteria and Virus-Like Particles along a Salinity Gradient in a Hypersaline Coastal Lagoon,” Aquatic Microbial Ecology, Vol. 54, No. 2, 2009, pp. 171-183. doi:10.3354/ame01262
[40]	C. Pedrós-Alió, J. I. Calderón-Paz, M. H. MacLean, G. Medina, C. Marrasé, J. M. Gasol and N. Guixa-Boixereu, “The Microbial Food Web along Salinity Gradients,” FEMS Microbiology Ecology, Vol. 32, No. 2, 2000, pp. 143-155.
[41]	S. Benlloch, A. Lopez-Lopez, E. O. Casamayor, L. Ovreas and V. Goddard, “Prokaryotic Genetic Diversity throughout the Salinity Gradient of a Coastal Solar Saltern,” Environmental Microbiology, Vol. 4, No. 6, 2002, pp. 349-360. doi:10.1046/j.1462-2920.2002.00306.x
[42]	J. P. Grime, “Competitive Exclusion in Herbaceous Vegetation,” Nature, Vol. 242, 1973, pp. 344-347. doi:10.1038/242344a0
[43]	H. S. Horn, “Markovian Properties of Forest Succession,” In: M. L. Cody and J. M. Diamond, Eds., Ecology and Evolution of Communities, Belknap Press, Cambridge, 1975, pp. 196-211.
[44]	J. H. Connell, “Diversity in Tropical Rain Forests and Coral Reefs,” Science, Vol. 199, No. 4335, 1978, pp. 1302-1310. doi:10.1126/science.199.4335.1302
[45]	W. P. Sousa, “Disturbance in Marine Intertidal Boulder Fields: The Nonequilibrium Maintenance of Species Diversity,” Ecology, Vol. 60, No. 6, 1979, pp. 1225-1239. doi:10.2307/1936969
[46]	M. Troussellier, H. Schafer, N. Batailler, L. Bernard, C. Courties, P. Lebaron, G. Muyzer, P. Servais and J. Vives-Rego, “Bacterial Activity and Genetic Richness along an Estuarine Gradient (Rhone River plume, France),” Aquatic Microbial Ecology, Vol. 28, No. 1, 2002, pp. 13-24. doi:10.3354/ame028013
[47]	K. Muylaert, K. Sabbe and W. Vyverman, “Changes in Phytoplankton Diversity and Community Composition along the Salinity Gradient of the Schelde estuary (Belgium/The Netherlands),” Estuarine, Coastal and Shelf Science, Vol. 82, No. 2, 2009, pp. 335-340. doi:10.1016/j.ecss.2009.01.024
[48]	I. V. Telesh, H. Schubert and S. O. Skarlato, “Revisiting Remane’s Concept: Evidence for High Plankton Diversity and a Protistan Species Maximum in the Horohalinicum of the Baltic Sea,” Marine Ecology Progress Series, Vol. 421, 2011, pp. 1-11. doi:10.3354/meps08928