Methanogenesis may represent a key process in the terminal phases of anaerobic organic matter mineralization in sediments of coastal lagoons. The aim of the present work was to study the temporal and spatial dynamics of methanogenic archaea in sediments of tropical coastal lagoons and their relationship with environmental changes in order to determine how these influence methanogenic community. Sediment samples were collected during the dry (February, May, and early June) and rainy seasons (July, October, and November). Microbiological analysis included the quantification of viable methanogenic archaea (MA) with three substrates and the evaluation of kinetic activity from acetate in the presence and absence of sulfate. The environmental variables assessed were temperature, pH, Eh, salinity, sulfate, solids content, organic carbon, and carbohydrates. MA abundance was significantly higher in the rainy season (106–107？cells/g) compared with the dry season (104–106？cells/g), with methanol as an important substrate. At spatial level, MA were detected in the two layers analyzed, and no important variations were observed either in MA abundance or activity. Salinity, sulfate, solids, organic carbon, and Eh were the environmental variables related to methanogenic community. A conceptual model is proposed to explain the dynamics of the MA. 1. Introduction Coastal and marine environments, including estuaries and coastal lagoons, are characterized by large amounts of organic matter, which is mineralized primarily in sediments through anaerobic processes, sulfate reduction being the dominant metabolic pathway [1, 2]. However, although these ecosystems are the typical habitat of sulfate-reducing prokaryotes (SRP), methanogenic archaea (MA) and methane production have also been detected [3, 4]. MA are strict anaerobes that produce methane as end-product of their metabolism. These organisms are common in anoxic environments in which electron acceptors such as nitrate and sulfate are either absents or present at low concentrations and are usually dominant in freshwater environments. In the presence of these electron acceptors, methanogenesis is outcompeted by anaerobic respiration, mainly for thermodynamic reasons [5]. MA distribution patterns and its number, as well as physical, chemical, and nutritional parameters controlling their abundance and distribution have been studied in lacustrine sediments [6] and in coastal environments [7, 8]. Most of the ecological studies assessing the structure of methanogenic communities in estuarine systems have been performed in
References
[1]
B. B. J？rgensen, “Mineralization of organic matter in the sea bed—the role of sulphate reduction,” Nature, vol. 296, no. 5858, pp. 643–645, 1982.
[2]
M. Fukui, J. Suh, Y. Yonezawa, and Y. Urushigawa, “Major substrates for microbial sulfate reduction in the sediments of Ise Bay, Japan,” Ecological Research, vol. 12, no. 2, pp. 201–209, 1997.
[3]
D. Marty, P. Bonin, V. Michotey, and M. Bianchi, “Bacterial biogas production in coastal systems affected by freshwater inputs,” Continental Shelf Research, vol. 21, no. 18-19, pp. 2105–2115, 2001.
[4]
D. E. Canfield, E. Kristensen, and B. Thamdrup, “The methane cycle,” in Advances in Marine Biology. Aquatic Geomicrobiology, A. Southward, P. A. Tyler, C. M. Young, and L. A. Fuiman, Eds., vol. 48, chapter 10, pp. 383–418, Elsevier, London, UK, 2005.
[5]
R. K. Thauer, A. K. Kaster, H. Seedorf, W. Buckel, and R. Hedderich, “Methanogenic archaea: ecologically relevant differences in energy conservation,” Nature Reviews Microbiology, vol. 6, no. 8, pp. 579–591, 2008.
[6]
K. Zepp Falz, C. Holliger, R. Gro？kopf et al., “Vertical distribution of methanogens in the anoxic sediment of Rotsee (Switzerland),” Applied and Environmental Microbiology, vol. 65, no. 6, pp. 2402–2408, 1999.
[7]
K. J. Purdy, M. A. Munson, D. B. Nedwell, and T. M. Embley, “Comparison of the molecular diversity of the methanogenic community at the brackish and marine ends of a UK estuary,” FEMS Microbiology Ecology, vol. 39, no. 1, pp. 17–21, 2002.
[8]
R. Wilms, H. Sass, B. K？pke, J. K？ster, H. Cypionka, and B. Engelen, “Specific Bacterial, Archaeal, and Eukaryotic communities in tidal-flat sediments along a vertical profile of several meters,” Applied and Environmental Microbiology, vol. 72, no. 4, pp. 2756–2764, 2006.
[9]
M. J. Franklin, J. W. William, and W. B. Whitman, “Populations of methanogenic bacteria in a Georgia salt marsh,” Applied and Environmental Microbiology, vol. 54, no. 5, pp. 1151–1157, 1988.
[10]
M. A. Munson, D. B. Nedwell, and T. M. Embley, “Phylogenetic diversity of Archaea in sediment samples from a coastal salt marsh,” Applied and Environmental Microbiology, vol. 63, no. 12, pp. 4729–4733, 1997.
[11]
R. Segers and S. W. M. Kengen, “Methane production as a function of anaerobic carbon mineralization: a process model,” Soil Biology and Biochemistry, vol. 30, no. 8-9, pp. 1107–1117, 1998.
[12]
S. Takii and M. Fukui, “Relative importance of methanogenesis, sulfate reduction and denitrification in sediments of the lower Tama river,” Bulletin of Japanese Society of Microbial Ecology, vol. 6, no. 1, pp. 9–17, 1991.
[13]
K. J. Purdy, M. A. Munson, T. Cresswell-Maynard, D. B. Nedwell, and T. M. Embley, “Use of 16S rRNA-targeted oligonucleotide probes to investigate function and phylogeny of sulphate-reducing bacteria and methanogenic archaea in a UK estuary,” FEMS Microbiology Ecology, vol. 44, no. 3, pp. 361–371, 2003.
[14]
T. Ramamurthy, R. Mohanraju, and R. Natarajan, “Distribution and ecology of methanogenic bacteria in mangrove sediments of Pitchavaram, east coast of India,” Indian Journal of Marine Sciences, vol. 19, no. 4, pp. 269–273, 1990.
[15]
R. Mohanraju and R. Natarajan, “Methanogenic bacteria in mangrove sediments,” Hydrobiologia, vol. 247, no. 1–3, pp. 187–193, 1992.
[16]
H. Biswas, S. K. Mukhopadhyay, S. Sen, and T. K. Jana, “Spatial and temporal patterns of methane dynamics in the tropical mangrove dominated estuary, NE coast of Bay of Bengal, India,” Journal of Marine Systems, vol. 68, no. 1-2, pp. 55–64, 2007.
[17]
INE-SEMARNAP, Programa de Manejo Reserva de la Biósfera La Encrucijada, Instituto Nacional de Ecología-Secretaría del Medio Ambiente, Recursos Naturales y, Pesca, Mexico, 1999.
[18]
F. J. Flores-Verdugo, F. González-Farías, D. S. Zamorano, and P. Ramírez-García, “Mangrove ecosystems of the Pacific Coast of Mexico: distribution, structure, litter fall, and detritus dynamics,” in Coastal Plant Communities of Latin America, U. Seliger, Ed., vol. 17, pp. 269–288, Academic Press, New York, NY, USA, 1992.
[19]
F. J. Flores-Verdugo, G. de la Lanza-Espino, F. Contreras-Espinosa, and C. M. Agraz-Hernández, “The tropical Pacific Coast of Mexico,” in Coastal Marine Ecosystems of Latin American, Ecological Studies, U. Seliger and B. Kjerve, Eds., vol. 144, pp. 307–314, Springer, Berlin, Germany, 2001.
[20]
D. Langmuir, “Eh-pH determination,” in Proceedings Sediments and Petrology, R. E. Conver, Ed., p. 653, Wiley-Interscience, New York, NY, USA, 1971.
[21]
W. E. Balch, G. E. Fox, L. J. Magrum, C. R. Woese, and R. S. Wolfe, “Methanogens: reevaluation of a unique biological group,” Microbiological Reviews, vol. 43, no. 2, pp. 260–296, 1979.
[22]
B. L. Howes, “Effects of sampling technique on measurements of porewater constituents in salt marsh sediments,” Limnology and Oceanography, vol. 30, no. 1, pp. 221–227, 1985.
[23]
R. W. Howarth, “A rapid and precise method for determining sulfate in seawater, estuarine waters, and sediment pore waters,” Limnology and Oceanography, vol. 23, no. 5, pp. 1066–1069, 1978.
[24]
M. Dubois, K. A. Gilles, J. K. Hamilton, P. A. Rebers, and F. Smith, “Colorimetric method for determination of sugars and related substances,” Analytical Chemistry, vol. 28, no. 3, pp. 350–356, 1956.
[25]
APHA, AWWA, and WPCF, Eds., Standard Methods For the Examination of Water and Wastewater, American Public Health Association, American Water Works Association and Water Pollution Control Federation, Washington, DC, USA, 2005.
[26]
H. Gaudette, W. Fligh, L. Toner, and D. Folger, “An inexpensive titration method for the determination of organic carbon in recent sediments,” Journal of Sediments and Petrology, vol. 44, no. 1, pp. 249–253, 1974.
[27]
J. H. Zar, Bioestatistical Analysis, Prentice Hall, New York, NY, USA, 1999.
[28]
C. J. F. Ter Braak, “Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis,” Ecology, vol. 67, no. 5, pp. 1167–1179, 1986.
[29]
E. Lallier-Vergès, B. P. Perrussel, J. R. Disnar, and F. Baltzer, “Relationships between environmental conditions and the diagenetic evolution of organic matter derived from higher plants in a modern mangrove swamp system (Guadeloupe, French West Indies),” Organic Geochemistry, vol. 29, no. 5–7, pp. 1663–1686, 1998.
[30]
B. Knoppers and B. Kjerfve, “Coastal lagoons of Southeastern Brazil: physical and biogeochemical characteristics,” in Estuaries of South America, G. M. E. Perillo, M. C. Piccolo, and M. Pino-Quivira, Eds., pp. 35–66, Springer, New York, NY, USA, 1997.
[31]
M. R. Preston and P. Prodduturu, “Tidal variations of particulate carbohydrates in the Mersey estuary,” Estuarine, Coastal and Shelf Science, vol. 34, no. 1, pp. 37–48, 1992.
[32]
R. W. Howarth, “Microbial processes in salt-marsh sediments,” in Aquatic Microbiology, T. E. Ford, Ed., pp. 239–260, Blackwell Scientific Publications, Boston, Mass, USA, 1993.
[33]
A. L. dos Santos Fonseca, M. Minello, C. Cardoso Marinho, and F. de Assis Esteves, “Methane concentration in water column and in pore water of a coastal lagoon (Cabiúnas Lagoon, Macaé, RJ, Brazil),” Brazilian Archives of Biology and Technology, vol. 47, no. 2, pp. 301–308, 2004.
[34]
A. Verma, V. Subramanian, and R. Ramesh, “Methane emissions from a coastal lagoon: vembanad Lake, West Coast, India,” Chemosphere, vol. 47, no. 8, pp. 883–889, 2002.
[35]
T. Egli, “The ecological and physiological significance of the growth of heterotrophic microorganisms with mixtures of substrates,” in Advances in Microbial Ecology, J. Gwynfryn, Ed., vol. 14, pp. 305–386, Plenum Press, New York, NY, USA, 1995.
[36]
R. Conrad, “Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments,” FEMS Microbiology Ecology, vol. 28, no. 3, pp. 193–202, 1999.
[37]
M. Holmer and E. Kristensen, “Coexistence of sulfate reduction and methane production in an organic-rich sediment,” Marine Ecology Progress Series, vol. 107, no. 1-2, pp. 177–184, 1994.
[38]
H. T. S. Boschker, W. de Graaf, M. K？ster, L. A. Meyer-Reil, and T. E. Cappenberg, “Bacterial populations and processes involved in acetate and propionate consumption in anoxic brackish sediment,” FEMS Microbiology Ecology, vol. 35, no. 1, pp. 97–103, 2001.
[39]
M. R. Torres-Alvarado, Determinación de la diversidad y actividad bacteriana sulfatorreductora y metanogénica en los sedimentos de dos ecosistemas estuarino-lagunares del Estado de Chiapas [Ph.D. thesis], Universidad Autónoma Metropolitana-Iztapalapa, México, Mexico, 2009.
[40]
H. K. Kludze and R. D. DeLaune, “Methane emissions and growth of Spartina patens in response to soil redox intensity,” Soil Science Society of America Journal, vol. 58, no. 6, pp. 1838–1845, 1994.
