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Structure and Functional Properties of Bacterial Communities in Surface Sediments of the Recently Declared Nutrient-Saturated Lake Villarrica in Southern Chile

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Abstract

Lake Villarrica, one of Chile’s main freshwater water bodies, was recently declared a nutrient-saturated lake due to increased phosphorus (P) and nitrogen (N) levels. Although a decontamination plan based on environmental parameters is being established, it does not consider microbial parameters. Here, we conducted high-throughput DNA sequencing and quantitative polymerase chain reaction (qPCR) analyses to reveal the structure and functional properties of bacterial communities in surface sediments collected from sites with contrasting anthropogenic pressures in Lake Villarrica. Alpha diversity revealed an elevated bacterial richness and diversity in the more anthropogenized sediments. The phylum Proteobacteria, Bacteroidetes, Acidobacteria, and Actinobacteria dominated the community. The principal coordinate analysis (PCoA) and redundancy analysis (RDA) showed significant differences in bacterial communities of sampling sites. Predicted functional analysis showed that N cycling functions (e.g., nitrification and denitrification) were significant. The microbial co-occurrence networks analysis suggested Chitinophagaceae, Caldilineaceae, Planctomycetaceae, and Phycisphaerae families as keystone taxa. Bacterial functional genes related to P (phoC, phoD, and phoX) and N (nifH and nosZ) cycling were detected in all samples by qPCR. In addition, an RDA related to N and P cycling revealed that physicochemical properties and functional genes were positively correlated with several nitrite-oxidizing, ammonia-oxidizing, and N-fixing bacterial genera. Finally, denitrifying gene (nosZ) was the most significant factor influencing the topological characteristics of co-occurrence networks and bacterial interactions. Our results represent one of a few approaches to elucidate the structure and role of bacterial communities in Chilean lake sediments, which might be helpful in conservation and decontamination plans.

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Acknowledgements

The authors acknowledge to the Scientific and Technological Bioresource Nucleus (BIOREN) for the availability of Illumina MiSeq equipment (Fondequip, code EQM150126). The authors would also like to thank (1) “Dirección General del Territorio Marítimo y de Marina Mercante (DIRECTEMAR)” of Pucón city, (2) Biol. Bárbara Cisternas from ‘Gobernación Marítima’ of Valdivia city, and (3) Eng. Pablo Etcharren from Seremi del Medio Ambiente (Región de La Araucanía) of the Ministerio de Medio Ambiente de Chile provided support for selecting sampling sites and collecting sediment samples. Finally, the authors would like to acknowledge the Editor and two anonymous reviewers for their criticism reading and constructive commentaries, which improved the quality of our manuscript.

Funding

This study was funded by Chile-China Joint Projects on Water Resources Management from ANID and NSFC (NSFC190012 in Chile and Grant No. 51961125201 in China) (to M.A.C., J.J.A., E.C., C.R., J.B., L.Z., R.X. and M.A.J.), by International Cooperation Project Chile-USA from ANID (code REDES190079) (to, M.A.C., J.J.A., J.I.R., A.H., D.P.J., A.O. and M.A.J.), by FONDECYT project no. 1201386 and 1221228 (to J.J.A. and M.A.J.), by NSFC (42077386) (Q.Z.), and by Science and Technology Research Partnership for Sustainable Development (SATREPS, Japan) (code JPMJSA1705) (to M.A.C., J.J.A, J.I.R., T.R. and M.A.J.).

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Author notes

  1. Marco A. Campos and Qian Zhang  have contributed equally to this work.

Authors and Affiliations

  1. Laboratorio de Ecología Microbiana Aplicada (EMALAB), Departamento de Ciencias Químicas y Recursos Naturales, Universidad de La Frontera, Ave. Francisco Salazar, 01145, Temuco, Chile

    Marco A. Campos, Jacquelinne J. Acuña, Joaquin I. Rilling, Tay Ruiz, Elizabeth Carrazana, Cristóbal Reyno & Milko A. Jorquera

  2. Scientific and Technological Bioresource Nucleus (BIOREN), Universidad de La Frontera, Ave. Francisco Salazar, 01145, Temuco, Chile

    Marco A. Campos, Jacquelinne J. Acuña, Joaquin I. Rilling, Tay Ruiz, Elizabeth Carrazana, Cristóbal Reyno & Milko A. Jorquera

  3. The BioTechnology Institute, University of Minnesota, 140 Gortner Lab, 1479 Gortner Ave., St Paul, MN, 55108-6106, USA

    Qian Zhang, Mikael Elias & Michael J Sadowsky

  4. Fujian Provincial Key Laboratory for Coastal Ecology and Environmental Studies, College of the Environment and Ecology, Xiamen University, Xiamen, 361100, People’s Republic of China

    Qian Zhang

  5. Doctorado en Ciencias de Recursos Naturales, Universidad de La Frontera, Ave. Francisco Salazar, 01145, Temuco, Chile

    Tay Ruiz

  6. Doctorado en Ciencias mención Biología Celular y Molecular Aplicada, Universidad de La Frontera, Ave. Francisco Salazar, 01145, Temuco, Chile

    Elizabeth Carrazana & Cristóbal Reyno

  7. Department of Plant and Soil Sciences, University of Delaware, Newark, DE, 19716, USA

    Anthony Hollenback, Katelyn Gray & Deb P. Jaisi

  8. Soil and Water Sciences Department, University of Florida, PO Box 110290, Gainesville, FL, 32608-32611, USA

    Andrew Ogram

  9. State Key Laboratory of Water Environment Simulation, School of Environment, Beijing Normal University, Beijing, 100875, China

    Junhong Bai & Ling Zhang

  10. College of Environment and Safety Engineering, Fuzhou University, Fuzhou, 350108, China

    Rong Xiao

  11. Department of Biochemistry, Molecular Biology and Biophysics, University of Minnesota, 140 Gortner Lab, 1479 Gortner Ave., St Paul, MN, 55108-6106, USA

    Mikael Elias

  12. College of the Environment & Ecology, Xiamen University, Xiamen, 361100, People’s Republic of China

    Jingming Hu

Authors
  1. Marco A. Campos
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  2. Qian Zhang
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  3. Jacquelinne J. Acuña
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  17. Jingming Hu
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  18. Milko A. Jorquera
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by M.A.C., Q.Z., J.J.A., J.I.R., T.R., E.C., C.R., and J.H. The first draft of the manuscript was written by M.A.C., Q.Z., and M.A.J. All authors commented, revised, and edited on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Milko A. Jorquera.

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Campos, M.A., Zhang, Q., Acuña, J.J. et al. Structure and Functional Properties of Bacterial Communities in Surface Sediments of the Recently Declared Nutrient-Saturated Lake Villarrica in Southern Chile. Microb Ecol 86, 1513–1533 (2023). https://doi.org/10.1007/s00248-023-02173-2

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