Abstract
The process of chemosynthesis can represent an important source of organic matter and energy across the benthic zone. However, its detailed vertical distribution and importance in relation to other microbial processes are still poorly investigated in inland aquatic ecosystems. Here, we determined the rates of dark inorganic carbon fixation (DCF) compared to heterotrophic bacterial production (BP) and oxygen consumption (SOC) across a depth profile of oxic to anoxic sediments in the littoral zone of nine tropical lakes located in one of the most important coastal conservation areas, the Jurubatiba Sandbank National Park (Rio de Janeiro, Brazil). Rates of DCF were highly variable (means of 0.1–1.2 mmol C m−2 d−1) among the studied lakes, with mostly production occurring below 10 mm of sediment in the anoxic zone. Although presenting a relatively low contribution in relation to BP and SOC, our study showed extensive microbial metabolism in the anaerobic sediment below the top centimeter, highlighting the importance of studying microbial processes across depth at fine scales. To our knowledge, it is the first study to show detailed vertical DCF rates in coastal tropical lake sediments, thus contributing to a better comprehension of the microbial role in the biogeochemical cycles of aquatic systems.
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References
Andersen K, Kjar T, Revsbech NP (2001) An oxygen insensitive microsensor for nitrous oxide. Sensor Actuat B Chem 81:42–48. https://doi.org/10.1016/S0925-4005(01)00924-8
Battin TJ, Kaplan LA, Findlay S, Hopkinson CS, Marti E, Packman AI, Newbold JD, Sabater F (2009) Biophysical controls on organic carbon fluxes in fluvial networks. Nat Geosci 2:595–595. https://doi.org/10.1038/ngeo602
Boschker HTS, Vasquez-Cardenas D, Bolhuis H, Moerdijk-Poortvliet TWC, Moodley L (2014) Chemoautotrophic carbon fixation rates and active bacterial communities in intertidal marine sediments. PLoS ONE 9(7):e101443. https://doi.org/10.1371/journal.pone.0101443
Buesing N, Marxsen J (2005) Theoretical and empirical conversion factors for determining bacterial production in freshwater sediments via leucine incorporation. Limnol Oceanogr Meth 3:101–107. https://doi.org/10.4319/lom.2005.3.101
Caliman A, Carneiro LS, Santangelo JM, Guariento RD, Pires APF, Suhett AL, Quesado LB, Scofield V, Fonte ES, Lopes PM, Sanches LF, Azevedo FD, Marinho CC, Bozelli RL, Esteves FA, Farjalla VF (2010) Temporal coherence among tropical coastal lagoons: a search for patterns and mechanisms. Braz J Biol 70(3 Suppl):803–814. https://doi.org/10.1590/S1519-69842010000400011
Camacho A, Erez J, Chicote A, Florín M, Squires MM, Lehmann C, Backofen R (2001) Microbial microstratification, inorganic carbon photoassimilation and dark carbon fixation at the chemocline of the meromictic Lake Cadagno (Switzerland) and its relevance to the food web. Aquat Sci 63:91–106. https://doi.org/10.1007/PL00001346
Carmouze JP, Knoppers B, Vasconcelos P (1991) Metabolism of a subtropical Brazilian lagoon. Biogeochemistry 14:129–148. https://doi.org/10.1007/BF00002902
Casamayor EO (2010) Vertical distribution of planktonic autotrophic thiobacilli and dark CO2 fixation rates in lakes with oxygen–sulfide interfaces. Aquat Microb Ecol 59:217–228. https://doi.org/10.3354/ame01399
Casamayor EO, García-Cantizano J, Pedrós-Alió C (2008) Carbon dioxide fixation in the dark by photosynthetic bacteria in sulfide-rich stratified lakes with oxic-anoxic interfaces. Limnol Oceanogr 53:1193–1203. https://doi.org/10.4319/lo.2008.53.4.1193
Casamayor EO, Lliros M, Picazo A, Barberan A, Borrego CM, Camacho A (2012) Contribution of deep dark fixation processes to overall CO2 incorporation and large vertical changes of microbial populations in stratified karstic lakes. Aquat Sci 74:61–75. https://doi.org/10.1007/s00027-011-0196-5
Chuang P-C, Young MB, Dale AW, Miller LG, Herrera-Silveira JA, Paytan A (2017) Methane fluxes from tropical coastal lagoons surrounded by mangroves Yucatán, Mexico. J Geophys Res Biogeosci 122:1156–1174. https://doi.org/10.1002/2017JG003761
Cole JJ, Findlay S, Pace ML (1988) Bacterial production in fresh and saltwater ecosystems: A cross-system overview. Mar Ecol Prog Ser 43:1–10
Cole JJ, Prairie YT, Caraco NF, McDowell WH, Tranvik LJ, Striegl RG, Duarte CM, Kortelainen P, Downing JA, Middelburg JJ, Melack J (2007) Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10:172–185. https://doi.org/10.1007/s10021-006-9013-8
da Cunha-Santino MB, Bianchini Júnior I (2003) Oxygen consumption during mineralization of organic compounds in water samples from a small sub-tropical reservoir (Brazil). Braz Arch Biol Technol 46(4):723–729. https://doi.org/10.1590/S1516-89132003000400027
Dean WE (1999) The carbon cycle and biogeochemical dynamics in lake sediments. J Paleolimnol 21:375–393. https://doi.org/10.1023/A:1008066118210
Dean WE, Gorham E (1998) Magnitude and significance of carbon burial in lakes, reservoirs, and peatlands. Geology 26:535–538. https://doi.org/10.1130/0091-7613(1998)026%3c0535:MASOCB%3e2.3.CO
Duyl FC, Kop AJ (1994) Bacterial production in North Sea sediments: clues to seasonal and spatial variations. Mar Biol 120:323–337. https://doi.org/10.1007/BF00349694
Enoksson V, Samuelsson M-O (1987) Nitrification and dissimilatory ammonium production and their effects on nitrogen flux over the sediment-water interface in bioturbated coastal sediments. Mar Ecol Prog Ser 36:181–189
Enrich-Prast A, Bastviken D, Crill P (2009) Chemosynthesis. In: Encyclopedia of Inland Waters, Elsevier, 211–225. https://doi.org/10.1016/B978-012370626-3.00126-5
Enrich-Prast A, Bastviken D, Crill P, Santoro AL, Signori CN, Sanseverino AM (2014) Chemosynthesis. In: Reference Module in Earth Systems and Environmental Sciences, Elsevier, 1–19. https://doi.org/10.1016/B978-0-12-409548-9.09054-0
Enrich-Prast A, Santoro AL, Coutinho RS, Nielsen LP, Esteves FA (2016a) a) Sediment denitrification in two contrasting tropical shallow lagoons. Estuar Coast 39:657–663. https://doi.org/10.1007/s12237-015-0017-5
Enrich-Prast A, Figueiredo V, Esteves FA, Nielsen LP (2016b) Controls of sediment nitrogen dynamics in tropical coastal lagoons. PLoS One 11(5):e0155586. https://doi.org/10.1371/journal.pone.0155586
Evrard V, Cook PLM, Veuger B, Huettel M, Middelburg JJ (2008) Tracing carbon and nitrogen incorporation and pathways in the microbial community of a photic subtidal sand. Aquat Microb Ecol 53:257–269. https://doi.org/10.3354/ame01248
Farjalla VF, Enrich-Prast A, Esteves FA, Cimbleris ACP (2006) Bacterial growth and DOC consumption in a tropical coastal lagoon. Braz J Biol 66(2A):383–392
Furtado ALS, Casper P, Esteves FA (2001) Bacterioplankton abundance, biomass and production in a Brazilian coastal lagoon and in two German lakes. An Acad Bras Cienc. https://doi.org/10.1590/S0001-37652001000100005
García-Cantizano J, Casamayor EO, Gasol JM, Guerrero R, Pedrós-Alió C (2005) Partitioning of CO2 incorporation among planktonic microbial guilds and estimation of in situ specific growth rates. Microb Ecol 50:230–241. https://doi.org/10.1007/s00248-004-0144-9
Glud RN, Gundersen JK, Ramsing NB (2000) Electrochemical and optical oxygen microsensors for in situ measurements. In: Buffle J, Horvai G (eds) In situ analytical techniques for water and sediment. John Wiley and Sons, Chichester, pp 19–75
Gudasz C, Bastviken D, Steger K, Premke K, Sobek S, Tranvik LJ (2010) Temperature-controlled organic carbon mineralization in lake sediments. Nature 466:478–481. https://doi.org/10.1038/nature09186
Hadas O, Pinkas R, Erez J (2001) High chemoautotrophic primary production in Lake Kinneret, Isreal: a neglected link in the carbon cycle of the lake. Limnol Oceanogr 46:1968–1976
Heinen EA, McManus J (2004) Carbon and nutrient cycling at the sediment-water boundary in western lake superior. J Great Lakes Res 30:113–132. https://doi.org/10.1016/S0380-1330(04)70381-0
Kornberg HL (1966) Anaplerotic sequences and their role in metabolism. In: Campbell PN, Greville GP (eds) Essays in Biochemistry. Academic Press, New York, pp 1–31
Kuuppo-Leinikki P, Salonen K (1992) Bacterioplankton in a small polyhumic lake with an anoxic hypolimnion. Hydrobiologia 229:159–168
Lau MP, Valerio G, Pilotti M, Hupfer M (2020) Intermittent meromixis controls the trophic state of warming deep lakes. Sci Rep 10:12928. https://doi.org/10.1038/s41598-020-69721-5
Lenk S, Arnds J, Zerjatke K, Musat N, Amann R, Mussmann M (2011) Novel groups of Gammaproteobacteria catalyse sulfur oxidation and carbon fixation in a coastal, intertidal sediment. Environ Microbiol 13:758–774
Markfoged R, Nielsen LP, Nyord T, Ottosen LDM, Revsbech NP (2011) Transient N2O accumulation and emission caused by O2 depletion in soil after liquid manure injection. Eur J Soil Sci 62:541–550. https://doi.org/10.1111/j.1365-2389.2010.01345.x
Molari M, Manini E, Dell’Anno A (2013) Dark inorganic carbon fixation sustains the functioning of benthic deep-sea ecosystems. Global Biogeochem Cycles 27:212–221. https://doi.org/10.1002/gbc.20030
Pace ML, Cole JJ (1994) Primary and bacterial production in lakes: are they coupled over depth? J Plankton Res 16(6):661–672. https://doi.org/10.1093/plankt/16.6.661
Pedrós-Alió C, Guerrero R (1993) Microbial ecology in Lake Cisó. Adv Microb Ecol 13:155–209
Revsbech NP (1989) An oxygen microsensor with a guard cathode. Limnol Oceanogr 34:474–478. https://doi.org/10.4319/lo.1989.34.2.0474
Santoro AL, Bastviken D, Gudasz C, Tranvik L, Enrich-Prast A (2013a) Dark carbon fixation: an important process in lake sediments. PLoS One 8:1–7. https://doi.org/10.1371/journal.pone.0065813
Santoro AL, Bastviken D, Tranvik L, Enrich-Prast A (2013b) Simultaneous measurements of dark carbon fixation and bacterial production in lake sediment. Limnol Oceanogr Methods 11:298–303. https://doi.org/10.4319/lom.2013.11.298
Signori CN, JP de S, Enrich-Prast A, (2020) Bacterial production prevails over photo- and chemosynthesis in a eutrophic tropical lagoon. Estuar Coast Shelf Sci 243:106889. https://doi.org/10.1016/j.ecss.2020.106889
Signori CN, Valentin JL, Pollery RCG, Enrich-Prast A (2017) Temporal variability of dark carbon fixation and bacterial production and their relation with environmental factors in a tropical estuarine system. Estuar Coast 40:2. https://doi.org/10.1007/s12237-017-0338-7
Souza VF, Santoro AL, van Weerelt M, Enrich-Prast A (2012) Sediment denitrification, DNRA and anammox rates in tropical foodplain lake (Pantanal, Brazil). Oecol Aust 16:734–744. https://doi.org/10.4257/oeco.2012.1604.01
Sweerts JPRA, St. Louis V, Cappenberg TE (1989) Oxygen concentration profiles and exchange in sediment cores with circulated overlying water. Freshw Biol 21:401–409. https://doi.org/10.1111/j.1365-2427.1989.tb01372.x
Thomsen U, Kristensen E (1997) Dynamics of ∑CO2 in a surficial sandy marine sediment: The role of chemoautotrophy. Aquat Microb Ecol 12:165–176
Tranvik L, Downing JA, Cotner JB, Loiselle SA, Striegl RG, Ballatore TJ, Dillon P, Finlay K, Fortino K, Knoll LB (2009) Lakes and reservoirs as regulators of carbon cycling and climate. Limnol Oceanogr 54:2298–2314. https://doi.org/10.4319/lo.2009.54.6_part_2.2298
Verpoorter C, Kutser T, Seekell DA, Tranvik LJ (2014) A Global Inventory of Lakes Based on High-Resolution Satellite Imagery. Geophys Res Lett 41:6396–6402. https://doi.org/10.1002/2014GL060641
Acknowledgements
Ana Lucia Santoro received a STINT (Sweden) and CNPq (Brazil) scholarships at the time of sampling. The authors would like to thank the Brazilian funding agencies CNPq, CAPES, FAPERJ and FAPESP for different kinds of financial support throughout the process of sampling, evaluation and paper writing.
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The contributions of the authors were as follows: All authors conceived and designed the experiments. Ana Lucia Santoro performed the experiments and analyzed the data. Alex Enrich-Prast, David Bastviken and Lars Tranvik contributed with reagents/materials/analysis tools. All authors wrote and revised previous versions of the paper. All authors read and approved the final manuscript.
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Santoro, A.L., Enrich-Prast, A., Bastviken, D. et al. Spatial and vertical distribution of aerobic and anaerobic dark inorganic carbon fixation in coastal tropical lake sediments. Aquat Sci 83, 43 (2021). https://doi.org/10.1007/s00027-021-00803-w
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DOI: https://doi.org/10.1007/s00027-021-00803-w