Abstract
We studied the interaction between phototrophic and chemolithoautotrophic sulphide-oxidizing microorganisms in natural microbial mats forming in sulphidic streams. The structure of these mats varied between two end-members: one characterized by a layer dominated by large sulphur-oxidizing bacteria (SOB; mostly Beggiatoa-like) on top of a cyanobacterial layer (B/C mats) and the other with an inverted structure (C/B mats). C/B mats formed where the availability of oxygen from the water column was limited (<5 μm). Aerobic chemolithotrophic activity of the SOB depended entirely on oxygen produced locally by cyanobacteria during high light conditions. In contrast, B/C mats formed at locations where oxygen in the water column was comparatively abundant (>45 μM) and continuously present. Here SOB were independent of the photosynthetic activity of cyanobacteria and outcompeted the cyanobacteria in the uppermost layer of the mat where energy sources for both functional groups were concentrated. Outcompetition of photosynthetic microbes in the presence of light was facilitated by the decoupling of aerobic chemolithotrophy and oxygenic phototrophy. Remarkably, the B/C mats conserved much less energy than the C/B mats, although similar amounts of light and chemical energy were available. Thus ecosystems do not necessarily develop towards optimal energy usage. Our data suggest that, when two independent sources of energy are available, the structure and activity of microbial communities is primarily determined by the continuous rather than the intermittent energy source, even if the time-integrated energy flux of the intermittent energy source is greater.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Al-Najjar MAA, de Beer D, Jørgensen BB, Kühl M, Polerecky L . (2010). Conversion and conservation of light energy in a photosynthetic microbial mat ecosystem. ISME J 4: 440–449.
Al-Najjar MAA, de Beer D, Kühl M, Polerecky L . (2012). Light utilization efficiency in photosynthetic microbial mats. Environ Microbiol 14: 982–992.
Allwood AC, Grotzinger JP, Knoll AH, Burch IW, Anderson MS, Coleman ML et al. (2009). Controls on development and diversity of Early Archean stromatolites. Proc Natl Acad Sci USA 106: 9548–9555.
Anbar AD, Duan Y, Lyons TW, Arnold GL, Kendall B, Creaser RA et al. (2007). A whiff of oxygen before the great oxidation event? Science 317: 1903–1906.
Berg P, Risgaard-Petersen N, Rysgaard S . (1998). Interpretation of measured concentration profiles in sediment pore water. Limnol Oceanogr 43: 1500–1510.
Braman RS, Hendrix SA . (1989). Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium(III) reduction with chemiluminescence detection. Anal Chem 61: 2715–2718.
Buick R . (2008). When did oxygenic photosynthesis evolve? Philos Trans R Soc Lond B Biol Sci 363: 2731–2743.
Castresana J, Saraste M . (1995). Evolution of energetic metabolism: the respiration-early hypothesis. Trends Biochem Sci 20: 443–448.
Catling DC, Glein CR, Zahnle KJ, McKay CP . (2005). Why O2 is required by complex life on habitable planets and the concept of planetary 'oxygenation time'. Astrobiology 5: 415–438.
Cline JD . (1969). Oxygenation of hydrogen sulfide in seawater at constant salinity, temperature and pH. Environ Sci Technol 3: 838–843.
Cohen Y, Jørgensen BB, Revsbech NP, Poplawski R . (1986). Adaptation to hydrogen sulfide of oxygenic and anoxygenic photosynthesis among cyanobacteria. Appl Environ Microbiol 51: 398–407.
de Beer D, Schramm A, Santegoeds CM, Kühl M . (1997). A nitrite microsensor for profiling environmental biofilms. Appl Environ Microbiol 63: 973–977.
Dismukes GC, Klimov V V, Baranov S V, Kozlov YN, DasGupta J, Tyryshkin A . (2001). The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis. Proc Natl Acad Sci USA 98: 2170–2175.
Galdenzi S, Cocchioni M, Morichetti L, Amici V, Scuri S . (2008). Sulfidic ground-water chemistry in the Frasassi Caves, Italy. J Cave Karst Stud 70: 94–107.
Grotzinger JP, Knoll AH . (1999). Stromatolites in Precambrian carbonates: evolutionary mileposts or environmental dipsticks? Annu Rev Earth Planet Sci 27: 313–358.
Hall POJ, Aller RC . (1992). Rapid, small-volume, flow injection analysis for ∑(CO2) and NH4+ in marine and freshwaters. Limnol Oceanogr 37: 1113–1119.
Jeroschewski P, Steuckart C, Kühl M . (1996). An amperometric microsensor for the determination of H2S in aquatic environments. Anal Chem 68: 4351–4357.
Jørgensen BB, Cohen Y, Revsbech NP . (1986). Transition from anoxygenic to oxygenic photosynthesis in a Microcoleus chthonoplastes cyanobacterial mat. Appl Environ Microbiol 51: 408–417.
Jørgensen BB, Dunker R, Grünke S, Røy H . (2010). Filamentous sulfur bacteria, Beggiatoa spp., in arctic marine sediments (Svalbard, 79 degrees N). FEMS Microbiol Ecol 73: 500–513.
Klatt JM, Al-Najjar MAA, Yilmaz P, Lavik G, de Beer D, Polerecky L . (2015). Anoxygenic photosynthesis controls oxygenic photosynthesis in a cyanobacterium from a sulfidic spring. Appl Environ Microbiol AEM 81: 2025–2031.
Klatt JM, Polerecky L . (2015). Assessment of the stoichiometry and efficiency of CO2 fixation coupled to reduced sulfur oxidation. Front Microbiol 6: 484.
Lassen C, Ploug H, Jørgensen BB . (1992). A fibre-optic scalar irradiance microsensor: application for spectral light measurements in sediments. FEMS Microbiol Lett 86: 247–254.
Lyons TW, Reinhard CT, Planavsky NJ . (2014). The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506: 307–315.
Millero F . (1986). The thermodynamics and kinetics of the hydrogen sulfide system in natural waters. Mar Chem 18: 121–147.
Møller MM, Nielsen LP, Jørgensen BB . (1985). Oxygen responses and mat formation by Beggiatoa spp. Appl Environ Microbiol 50: 373–382.
Nelson DC, Jørgensen BB, Revsbech NP . (1986). Growth pattern and yield of a chemoautotrophic Beggiatoa sp. in oxygen-sulfide microgradients. Appl Environ Microbiol 52: 225–233.
Polerecky L, Bachar A, Schoon R, Grinstein M, Jørgensen BB, de Beer D et al. (2007). Contribution of Chloroflexus respiration to oxygen cycling in a hypersaline microbial mat from Lake Chiprana, Spain. Environ Microbiol 9: 2007–2024.
Polerecky L, Bissett A, Al-Najjar MAA, Färber P, Osmers H, Suci PA et al. (2009). Modular spectral imaging system for discrimination of pigments in cells and microbial communities. Appl Environ Microbiol 75: 758–771.
Revsbech NP, Jørgensen BB . (1983). Photosynthesis of benthic microflora measured with high spatial resolution by the oxygen microprofile method: capabilities and limitations of the method. Limnol Oceanogr 28: 749–759.
Revsbech NP . (1989). An oxygen microsensor with a guard cathode. Limnol Oceanogr 34: 474–478.
Schopf J . (2012). The fossil record of Cyanobacteria. In: Whitton BA (ed). Ecology of Cyanobacteria II. Springer: Dordrecht, Netherlands, pp 15–36.
Schwedt A, Kreutzmann A-C, Polerecky L, Schulz-Vogt HN . (2011). Sulfur respiration in a marine chemolithoautotrophic Beggiatoa strain. Front Microbiol 2: 276.
Seckbach J, Oren A (eds). (2010) Microbial Mats: Modern and Ancient Microorganisms in Stratified Systems. Springer: Dordrecht, Netherlands.
Sessions AL, Doughty DM, Welander PV, Summons RE, Newman DK . (2009). The continuing puzzle of the great oxidation event. Curr Biol 19: R567–R574.
Sherwood JE, Stagnitti F, Kokkinn MJ, Williams WD . (1991). Dissolved oxygen concentrations in hypersaline waters. Limnol Oceanogr 36: 235–250.
Tice MM, Lowe DR . (2004). Photosynthetic microbial mats in the 3,416-Myr-old ocean. Nature 431: 549–552.
Van der Meer MTJ, Schouten S, Bateson MM, Nübel U, Wieland A, Kühl M et al. (2005). Diel variations in carbon metabolism by green nonsulfur-like bacteria in alkaline siliceous hot spring microbial mats from Yellowstone National Park. Appl Environ Microbiol 71: 3978–3986.
Van Gemerden H, Mas J . (1995). Ecology of phototrophic sulfur bacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds). Anoxygenic Photosynthetic Bacteria, Advances in Photosynthesis and Respiration, Vol. 2. Springer Netherlands: Dordrecht, The Netherlands, pp 49–85.
Ward DM, Bauld J, Castenholz RW, Pierson BK . (1992). Modern phototrophic microbial mats: anoxygenic, intermittently oxygenic/anoxygenic, thermal, eukaryotic, and terrestrial. In: Schopf JW, Klein C (eds). The Proterozoic Biosphere: A Multidisciplinary Study. Cambridge University Press: NY, USA, pp 309–324.
Weber M, Färber P, Meyer V, Lott C, Eickert G, Fabricius KE et al. (2007). In situ applications of a new diver-operated motorized microsensor profiler. Environ Sci Technol 41: 6210–6215.
Wieland A, Kühl M . (2000). Short-term temperature effects on oxygen and sulfide cycling in a hypersaline cyanobacterial mat (Solar Lake, Egypt). Mar Ecol Prog Ser 196: 87–102.
Acknowledgements
We thank Daniel S Jones (University of Minnesota) for invaluable help in the field, Alessandro Montanari and Paula Metallo for providing laboratory facilities and enjoyable atmosphere at the Osservatorio Geologico di Coldigioco and Tim Ferdelman for fruitful discussions. We thank the technicians of the microsensor group for microsensor construction. This work was financially supported by the Max Planck Society, by a 2011 ‘For Women in Science Award’ to JMK and by NASA Astrobiology Institute (PSARC, NNA04CC06A) and Hanse-Wissenschaftskolleg Fellowship funds to JLM.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Additional information
Supplementary Information accompanies this paper on The ISME Journal website
Supplementary information
Rights and permissions
About this article
Cite this article
Klatt, J., Meyer, S., Häusler, S. et al. Structure and function of natural sulphide-oxidizing microbial mats under dynamic input of light and chemical energy. ISME J 10, 921–933 (2016). https://doi.org/10.1038/ismej.2015.167
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2015.167
This article is cited by
-
Photosynthetic performance in cyanobacteria with increased sulphide tolerance: an analysis comparing wild-type and experimentally derived strains
Photosynthesis Research (2022)
-
Possible link between Earth’s rotation rate and oxygenation
Nature Geoscience (2021)
-
Versatile cyanobacteria control the timing and extent of sulfide production in a Proterozoic analog microbial mat
The ISME Journal (2020)
-
Cyanobacterial photosynthesis under sulfidic conditions: insights from the isolate Leptolyngbya sp. strain hensonii
The ISME Journal (2018)
-
A penalty on photosynthetic growth in fluctuating light
Scientific Reports (2017)


