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Advances in the aquatic sciences
RESEARCH ARTICLE

Insights into the microbial autotrophic potential of a shallow oligotrophic alpine pond

Ilaria Mania https://orcid.org/0000-0001-8723-0930 A B , Martina Pellicciaro https://orcid.org/0000-0001-6778-723X A and Roberta Gorra https://orcid.org/0000-0002-7007-7113 A
+ Author Affiliations
- Author Affiliations

A Department of Agriculture, Forest and Food Sciences (DISAFA), University of Turin, Largo Braccini 2, I-10095 Grugliasco (Torino, TO), Italy.

B Corresponding author. Email: ilaria.mania@unito.it

Marine and Freshwater Research 72(6) 899-903 https://doi.org/10.1071/MF20241
Submitted: 6 August 2020  Accepted: 19 October 2020   Published: 16 December 2020

Abstract

Carbon dioxide fixation is one of the most important biogeochemical processes worldwide, but our current understanding of the distribution of microbial autotrophy and its ecological significance in oligotrophic freshwater systems, and particularly in benthic habitats, is poor and limited primarily to photoautotrophic organisms. In this study we investigated the autotrophic microbial communities inhabiting the sediments of a high-elevation, oligotrophic freshwater pond in the north-western Italian Alps. The abundance and distribution of three different forms of the ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) large-subunit gene (cbbLG, Form I green-like; cbbLR, Form I red-like; cbbM, Form II) were assessed in samples collected at different depths by quantitative polymerase chain reaction (qPCR); correlations with sediment geochemical properties and total bacterial abundance were also examined. RuBisCO forms cbbLG, cbbLR and cbbM were all detected, with abundances of 9.13–10.90, 6.93–8.77 and 6.75–7.93 log(copies) g–1 dry weight respectively. For all the RuBisCO genes, interannual variability overcame depth-related variability. The abundance of RuBisCO genes was strongly correlated with total bacterial abundance, and both were positively correlated with Ca2+ and Mg2+ concentrations. These observations provide some first indications of the distribution of photo- and chemolithoautotrophic bacteria relying on the Calvin–Benson–Bassham cycle for C fixation in alpine pond sediments, and suggest that they may represent an important component of the total benthic microbial community.

Keywords: primary production, qPCR, quantitative polymerase chain reaction, ribulose-1,5-bisphosphate carboxylase/oxygenase, RuBisCO, sediments.


References

Alfreider, A., Vogt, C., Hoffmann, D., and Babel, W. (2003). Diversity of ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit genes from groundwater and aquifer microorganisms. Microbial Ecology 45, 317–328.
Diversity of ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit genes from groundwater and aquifer microorganisms.Crossref | GoogleScholarGoogle Scholar | 12704564PubMed |

Andersson, I. (2008). Catalysis and regulation in RuBisCO. Journal of Experimental Botany 59, 1555–1568.
Catalysis and regulation in RuBisCO.Crossref | GoogleScholarGoogle Scholar | 18417482PubMed |

Badger, M. R., and Bek, E. J. (2008). Multiple RuBisCO forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. Journal of Experimental Botany 59, 1525–1541.
Multiple RuBisCO forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle.Crossref | GoogleScholarGoogle Scholar | 18245799PubMed |

Beniston, M. (2003). Climatic change in mountain regions: a review of possible impacts. Climatic Change 59, 5–31.
Climatic change in mountain regions: a review of possible impacts.Crossref | GoogleScholarGoogle Scholar |

Berg, I. A. (2011). Ecological aspects of the distribution of different autotrophic CO2 fixation pathways. Applied and Environmental Microbiology 77, 1925–1936.
Ecological aspects of the distribution of different autotrophic CO2 fixation pathways.Crossref | GoogleScholarGoogle Scholar | 21216907PubMed |

Colombo, N., Sambuelli, L., Comina, C., Colombero, C., Giardino, M., Gruber, S., Viviano, G., Vittori Antisari, L., and Salerno, F. (2018a). Mechanisms linking active rock glaciers and impounded surface water formation in high-mountain areas. Earth Surface Processes and Landforms 43, 417–431.
Mechanisms linking active rock glaciers and impounded surface water formation in high-mountain areas.Crossref | GoogleScholarGoogle Scholar |

Colombo, N., Gruber, S., Martin, M., Malandrino, M., Magnani, M., Godone, D., Freppaz, M., Fratianni, S., and Salerno, F. (2018b). Rainfall as primary driver of discharge and solute export from rock glaciers: the Col d’Olen Rock Glacier in the NW Italian Alps. The Science of the Total Environment 639, 316–330.
Rainfall as primary driver of discharge and solute export from rock glaciers: the Col d’Olen Rock Glacier in the NW Italian Alps.Crossref | GoogleScholarGoogle Scholar | 29791884PubMed |

Cremona, F., Laas, A., Arvola, L., Pierson, D., Nõges, P., and Nõges, T. (2016). Numerical exploration of the planktonic to benthic primary production ratios in lakes of the Baltic Sea Catchment. Ecosystems 19, 1386–1400.
Numerical exploration of the planktonic to benthic primary production ratios in lakes of the Baltic Sea Catchment.Crossref | GoogleScholarGoogle Scholar |

Dodds, W. K. (2003). The role of periphyton in phosphorus retention in shallow freshwater aquatic systems. Journal of Phycology 39, 840–849.
The role of periphyton in phosphorus retention in shallow freshwater aquatic systems.Crossref | GoogleScholarGoogle Scholar |

Dolhi, J. M., Teufel, A. G., Kong, W., and Morgan-Kiss, R. M. (2015). Diversity and spatial distribution of autotrophic communities within and between ice-covered Antarctic lakes (McMurdo Dry Valleys). Limnology and Oceanography 60, 977–991.
Diversity and spatial distribution of autotrophic communities within and between ice-covered Antarctic lakes (McMurdo Dry Valleys).Crossref | GoogleScholarGoogle Scholar |

Fischer, M. A., Güllert, S., Neulinger, S. C., Streit, W. R., and Schmitz, R. A. (2016). Evaluation of 16S rRNA gene primer pairs for monitoring microbial community structures showed high reproducibility within and low comparability between datasets generated with multiple archaeal and bacterial primer pairs. Frontiers in Microbiology 7, 1–15.
Evaluation of 16S rRNA gene primer pairs for monitoring microbial community structures showed high reproducibility within and low comparability between datasets generated with multiple archaeal and bacterial primer pairs.Crossref | GoogleScholarGoogle Scholar |

Glud, R. N., Woelfel, J., Karsten, U., Kühl, M., and Rysgaard, S. (2009). Benthic microalgal production in the Arctic: applied methods and status of the current database. Botanica Marina 52, 559–571.
Benthic microalgal production in the Arctic: applied methods and status of the current database.Crossref | GoogleScholarGoogle Scholar |

Kong, W., Dolhi, J. M., Chiuchiolo, A., Priscu, J., and Morgan-Kiss, R. M. (2012a). Evidence of Form II RuBisCO (cbbM) in a perennially ice-covered Antarctic lake. FEMS Microbiology Ecology 82, 491–500.
Evidence of Form II RuBisCO (cbbM) in a perennially ice-covered Antarctic lake.Crossref | GoogleScholarGoogle Scholar | 22703237PubMed |

Kong, W., Ream, D. C., Priscu, J. C., and Morgan-Kiss, R. M. (2012b). Diversity and expression of RuBisCO genes in a perennially ice-covered antarctic lake during the polar night transition. Applied and Environmental Microbiology 78, 4358–4366.
Diversity and expression of RuBisCO genes in a perennially ice-covered antarctic lake during the polar night transition.Crossref | GoogleScholarGoogle Scholar | 22492447PubMed |

Kong, W., Liu, J., Ji, M., Yue, L., Kang, S., and Morgan-Kiss, R. M. (2019). Autotrophic microbial community succession from glacier terminus to downstream waters on the Tibetan Plateau. FEMS Microbiology Ecology 95, fiz074.
Autotrophic microbial community succession from glacier terminus to downstream waters on the Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar | 31778180PubMed |

Lynn, T. M., Ge, T., Yuan, H., Wei, X., Wu, X., Xiao, K., Kumaresan, D., Yu, S. S., Wu, J., and Whiteley, A. S. (2017). Soil carbon-fixation rates and associated bacterial diversity and abundance in three natural ecosystems. Microbial Ecology 73, 645–657.
Soil carbon-fixation rates and associated bacterial diversity and abundance in three natural ecosystems.Crossref | GoogleScholarGoogle Scholar | 27838764PubMed |

Mania, I., Gorra, R., Colombo, N., Freppaz, M., Martin, M., and Anesio, A. M. (2019). Prokaryotic diversity and distribution in different habitats of an alpine rock glacier–pond system. Microbial Ecology 78, 70–84.
Prokaryotic diversity and distribution in different habitats of an alpine rock glacier–pond system.Crossref | GoogleScholarGoogle Scholar | 30317429PubMed |

Martinsen, K. T., Andersen, M. R., Kragh, T., and Sand-Jensen, K. (2017). High rates and close diel coupling of primary production and ecosystem respiration in small, oligotrophic lakes. Aquatic Sciences 79, 995–1007.
High rates and close diel coupling of primary production and ecosystem respiration in small, oligotrophic lakes.Crossref | GoogleScholarGoogle Scholar |

Paul, J. H., Alfreider, A., and Wawrik, B. (2000). Micro- and macrodiversity in rbcL sequences in ambient phytoplankton populations from the southeastern Gulf of Mexico. Marine Ecology Progress Series 198, 9–18.
Micro- and macrodiversity in rbcL sequences in ambient phytoplankton populations from the southeastern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |

Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., and Glöckner, F. O. (2012). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, D590–D596.
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools.Crossref | GoogleScholarGoogle Scholar | 23193283PubMed |

Redmond, L. E. (2018). Alpine limnology of the Rocky Mountains of Canada and the USA in the context of environmental change. Environmental Reviews 26, 231–238.
Alpine limnology of the Rocky Mountains of Canada and the USA in the context of environmental change.Crossref | GoogleScholarGoogle Scholar |

Selesi, D., Schmid, M., and Hartmann, A. (2005). Diversity of green-like and red-like ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit genes (cbbL) in differently managed agricultural soils. Applied and Environmental Microbiology 71, 175–184.
Diversity of green-like and red-like ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit genes (cbbL) in differently managed agricultural soils.Crossref | GoogleScholarGoogle Scholar | 15640185PubMed |

Slemmons, K. E. H., Saros, J. E., and Simon, K. (2013). The influence of glacial meltwater on alpine aquatic ecosystems: a review. Environmental Science. Processes & Impacts 15, 1794–1806.
The influence of glacial meltwater on alpine aquatic ecosystems: a review.Crossref | GoogleScholarGoogle Scholar |

Tabita, F. R. (1999). Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a different perspective. Photosynthesis Research 60, 1–28.
Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a different perspective.Crossref | GoogleScholarGoogle Scholar |

Tabita, F. R., Satagopan, S., Hanson, T. E., Kreel, N. E., and Scott, S. S. (2008). Distinct Form I, II, III, and IV RubisCO proteins from the three kingdoms of life provide clues about RubisCO evolution and structure/function relationships. Journal of Experimental Botany 59, 1515–1524.
Distinct Form I, II, III, and IV RubisCO proteins from the three kingdoms of life provide clues about RubisCO evolution and structure/function relationships.Crossref | GoogleScholarGoogle Scholar | 18281717PubMed |

Tiwari, A., Singh, P., Riyazat Khadim, S., Singh, A. K., Singh, U., Singh, P., and Ashtana, R. K. (2019). Role of Ca 2+ as protectant under heat stress by regulation of photosynthesis and membrane saturation in Anabaena PCC 7120. Protoplasma 256, 681–691.
Role of Ca 2+ as protectant under heat stress by regulation of photosynthesis and membrane saturation in Anabaena PCC 7120.Crossref | GoogleScholarGoogle Scholar | 30456698PubMed |

Tremblay, J., Singh, K., Fern, A., Kirton, E. S., He, S., Woyke, T., Lee, J., Chen, F., Dangl, J. L., and Tringe, S. G. (2015). Primer and platform effects on 16S rRNA tag sequencing. Frontiers in Microbiology 6, 1–15.
Primer and platform effects on 16S rRNA tag sequencing.Crossref | GoogleScholarGoogle Scholar |

Vadeboncoeur, Y., Jeppesen, E., Vander Zanden, M. J., Schierup, H.-H., Christoffersen, K., and Lodge, D. M. (2003). From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes. Limnology and Oceanography 48, 1408–1418.
From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes.Crossref | GoogleScholarGoogle Scholar |

Vesterinen, J., Devlin, S. P., Syväranta, J., and Jones, R. I. (2016). Accounting for littoral primary production by periphyton shifts a highly humic boreal lake towards net autotrophy. Freshwater Biology 61, 265–276.
Accounting for littoral primary production by periphyton shifts a highly humic boreal lake towards net autotrophy.Crossref | GoogleScholarGoogle Scholar |

Wan, Y., Bai, Y., He, J., Zhang, Y., Li, R., and Ruan, X. (2017). Temporal and spatial variations of aquatic environmental characteristics and sediment bacterial community in five regions of Lake Taihu. Aquatic Ecology 51, 343–358.
Temporal and spatial variations of aquatic environmental characteristics and sediment bacterial community in five regions of Lake Taihu.Crossref | GoogleScholarGoogle Scholar |

Watson, G. M. F., and Tabita, F. R. (1997). Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a molecule for phylogenetic and enzymological investigation. FEMS Microbiology Letters 146, 13–22.
Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a molecule for phylogenetic and enzymological investigation.Crossref | GoogleScholarGoogle Scholar |

Widder, S., Allen, R. J., Pfeiffer, T., Curtis, T. P., Wiuf, C., Sloan, W. T., Cordero, O. X., Brown, S. P., Momeni, B., Shou, W., Kettle, H., Flint, H. J., Haas, A. F., Laroche, B., Kreft, J-U., Rainey, P. B., Freilich, S., Schuster, S., Milferstedt, K., van der Meer, J. R., Großkopf, T., Huisman, J., Free, F., Picioreanu, C., Quince, C., Klapper, I., Labarthe, S., Smets, B. F., Wang, H., Isaac Newton Institute Fellows Soyer, O. K. (2016). Challenges in microbial ecology: building predictive understanding of community function and dynamics. The ISME Journal 10, 2557–2568.
Challenges in microbial ecology: building predictive understanding of community function and dynamics.Crossref | GoogleScholarGoogle Scholar | 27022995PubMed |

Yuan, H., Ge, T., Zou, S., Wu, X., Liu, S., Zhou, P., Chen, X., Brookes, P., and Wu, J. (2013). Effect of land use on the abundance and diversity of autotrophic bacteria as measured by ribulose-1,5-biphosphate carboxylase/oxygenase (RubisCO) large subunit gene abundance in soils. Biology and Fertility of Soils 49, 609–616.
Effect of land use on the abundance and diversity of autotrophic bacteria as measured by ribulose-1,5-biphosphate carboxylase/oxygenase (RubisCO) large subunit gene abundance in soils.Crossref | GoogleScholarGoogle Scholar |

Zhang, H., Yan, M., Huang, T., Huang, X., Yang, S., Li, N., and Wang, N. (2020). Water-lifting aerator reduces algal growth in stratified drinking water reservoir: novel insights into algal metabolic profiling and engineering applications. Environmental Pollution 266, 115384.
Water-lifting aerator reduces algal growth in stratified drinking water reservoir: novel insights into algal metabolic profiling and engineering applications.Crossref | GoogleScholarGoogle Scholar | 32829033PubMed |