Monitoring Diel Variations of Physiological Status and Bacterial Diversity in an Estuarine Microbial Mat: An Integrated Biomarker Analysis
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Microbial mats are highly productive microbial systems and a source of not-yet characterized microorganisms and metabolic strategies. In this article, we introduced a lipid biomarker/microbial isolation approach to detect short-term variations of microbial diversity, physiological and redox status, and also characterize lipid biomarkers from specific microbial groups that can be further monitored. Phospholipid fractions (PLFA) were examined for plasmalogens, indicative of certain anaerobes. The glycolipid fraction was processed for polyhydroxyalkanoates (PHA) and the neutral lipid fraction was used to evaluate respiratory quinone content. Data demonstrate an increase in the metabolic stress, unbalanced growth, proportion of anaerobic bacteria and respiratory rate after the maximal photosynthetic activity. Higher accumulation of polyhydroxyalkanoates at the same sampling point also suggested a situation of carbon storage by heterotrophs closely related to photosynthetic microorganisms. Besides, the characterization of lipid biomarkers (plasmalogens, sphingolipids) from specific microbial groups provided clues about the dynamics and diversity of less-characterized mat members. In this case, lipid analyses were complemented by the isolation and characterization of anaerobic spore formers and sulfate reducers to obtain insight into their affiliation and lipid composition. The results revealed that temporal shifts in lipid biomarkers are indicative of an intense change in the physiology, redox condition, and community composition along the diel cycle, and support the hypothesis that interactions between heterotrophs and primary producers play an important role in the carbon flow in microbial mats.
KeywordsSphingoid Base Respiratory Quinone Ebro Delta Neutral Lipid Fraction Total PLFA
This paper is dedicated to the memory of David C. White: “Thank you for being a friend and mentor, we will miss you.” We thank Mercè Piqueras and Wendy Ran for useful suggestions. We are grateful to the Center for Biomarker Analysis (TN, USA) staff for advice and technical assistance. This research was supported by Spanish MCyT grant BOS2002-02944 and MEC CGL2005-04990, and by grant DE-FC02-96ER62278, from the Office of Biological and Environmental Research (OBER) and the Natural and Accelerated Bioremediation Research (NABIR) Program. LV was recipient of a scholarship from the Spanish MECD (AP2001-0953).
- 5.Brisbarre, N, Fardeau, ML, Cueff, V, Cayol, JL, Barbier, G, Cilia, V, Ravot, G, Thomas, P, Garcia, JL, Ollivier, B (2003) Clostridium caminithermale sp. nov., a slightly halophilic and moderately thermophilic bacterium isolated from an Atlantic deep-sea hydrothermal chimney. Int J Syst Evol Microbiol 53: 1043–1049PubMedCrossRefGoogle Scholar
- 11.Geyer, R, Peacock, AD, White, DC, Lytle, C, Van Berkel, GJ (2004) Atmospheric pressure chemical ionization and atmospheric pressure photoionization for simultaneous mass spectrometric analysis of microbial respiratory ubiquinones and menaquinones. J Mass Spectrom 39: 922–929PubMedCrossRefGoogle Scholar
- 14.Guckert, JB, Antworth, CP, Nichols, PD, White, DC (1985) Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol Ecol 31: 147–158Google Scholar
- 21.Iwasaki, M, Hiraishi, A (1998) A new approach to numerical analyses of microbial quinone profiles in the environment. Microb Environ 13: 67–76Google Scholar
- 32.Mountfort, DO, Rainey, FA, Burghardt, J, Kaspar, HF, Stackebrandt, E (1997) Clostridium vincentii sp. nov., a new obligately anaerobic, saccharolytic, psychrophilic bacterium isolated from low-salinity pond sediment of the McMurdo Ice Shelf, Antarctica. Arch Microbiol 167: 54–60PubMedCrossRefGoogle Scholar
- 34.Navarrete, A, Urmeneta, J, Cantu, JM, Vegas, E, White, DC, Guerrero, R (2004) Signature lipid biomarkers of microbial mats of the Ebro delta (Spain), Camargue and Étang de Berre (France): an assessment of biomass and activity. Ophelia 58: 175–188Google Scholar
- 40.Spring, S, Merkhoffer, B, Weiss, N, Kroppenstedt, RM, Hippeand, H, Stackebrandt, E (2003) Characterization of novel psychrophilic clostridia from an Antarctic microbial mat: description of Clostridium frigoris sp. nov., Clostridium lacusfryxellense sp. nov., Clostridium bowmanii sp. nov. and Clostridium psychrophilum sp. nov. and reclassification of Clostridium laramiense as Clostridium estertheticum subsp. laramiense subsp. nov. Int J Syst Evol Microbiol 53: 1019–1029PubMedCrossRefGoogle Scholar
- 42.Villanueva, L, Navarrete, A, Urmeneta, J, White, DC, Guerrero, R (2004) Combined phospholipid biomarker-16S rRNA gene denaturing gradient gel electrophoresis analysis of bacterial diversity and physiological status in an intertidal microbial mat. Appl Environ Microbiol 70: 6920–6926PubMedCrossRefGoogle Scholar
- 43.White, DC, Bobbie, RJ, Heron, JS, King, JD, Morrison, SJ (1979) Biochemical measurements of microbial mass and activity from environmental samples. In: Costerton, JW, Colwell, RR (Eds.) Native Aquatic Bacteria: Enumeration, Activity and Ecology. ASTM STP 695, American Society for Testing and Materials, Philadelphia, PA, pp 69–81Google Scholar
- 45.Wilkinson, SG (1988) Gram-negative bacteria. In: Ratledge, C, Wilkinson, SG (Eds.) Microbial Lipids, Academic Press, London, UK, pp 299–488Google Scholar