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

Marco A. Campos; Qian Zhang; Jacquelinne J. Acuña; Joaquin I. Rilling; Tay Ruiz; Elizabeth Carrazana; Cristóbal Reyno; Anthony Hollenback; Katelyn Gray; Deb P. Jaisi; Andrew Ogram; Junhong Bai; Ling Zhang; Rong Xiao; Mikael Elias; Michael J. Sadowsky; Jingming Hu; Milko A. Jorquera

doi:10.1007/s00248-023-02173-2

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

Marco A. Campos, Qian Zhang, Jacquelinne J. Acuña, Joaquin I. Rilling, Tay Ruiz, Elizabeth Carrazana, Cristóbal Reyno, Anthony Hollenback, Katelyn Gray, Deb P. Jaisi, Andrew Ogram, Junhong Bai, Ling Zhang, Rong Xiao, Mikael Elias, Michael J. Sadowsky, Jingming Hu, Milko A. Jorquera

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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.

Original language	English (US)
Pages (from-to)	1513-1533
Number of pages	21
Journal	Microbial ecology
Volume	86
Issue number	3
DOIs	https://doi.org/10.1007/s00248-023-02173-2
State	Published - Oct 2023

Bibliographical note

Funding Information:
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.).

Publisher Copyright:
© 2023, The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Keywords

Bacterial communities
Bacterial diversity
Community structure
Functional genes
Lake sediments
Nutrients

PubMed: MeSH publication types

Journal Article

Publisher link

10.1007/s00248-023-02173-2

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Campos, M. A., Zhang, Q., Acuña, J. J., Rilling, J. I., Ruiz, T., Carrazana, E., Reyno, C., Hollenback, A., Gray, K., Jaisi, D. P., Ogram, A., Bai, J., Zhang, L., Xiao, R., Elias, M., Sadowsky, M. J., Hu, J., & Jorquera, M. A. (2023). Structure and Functional Properties of Bacterial Communities in Surface Sediments of the Recently Declared Nutrient-Saturated Lake Villarrica in Southern Chile. Microbial ecology, 86(3), 1513-1533. https://doi.org/10.1007/s00248-023-02173-2

Campos, MA, Zhang, Q, Acuña, JJ, Rilling, JI, Ruiz, T, Carrazana, E, Reyno, C, Hollenback, A, Gray, K, Jaisi, DP, Ogram, A, Bai, J, Zhang, L, Xiao, R, Elias, M , Sadowsky, MJ, Hu, J & Jorquera, MA 2023, 'Structure and Functional Properties of Bacterial Communities in Surface Sediments of the Recently Declared Nutrient-Saturated Lake Villarrica in Southern Chile', Microbial ecology, vol. 86, no. 3, pp. 1513-1533. https://doi.org/10.1007/s00248-023-02173-2

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

abstract = "Lake Villarrica, one of Chile{\textquoteright}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.",

keywords = "Bacterial communities, Bacterial diversity, Community structure, Functional genes, Lake sediments, Nutrients",

author = "Campos, {Marco A.} and Qian Zhang and Acu{\~n}a, {Jacquelinne J.} and Rilling, {Joaquin I.} and Tay Ruiz and Elizabeth Carrazana and Crist{\'o}bal Reyno and Anthony Hollenback and Katelyn Gray and Jaisi, {Deb P.} and Andrew Ogram and Junhong Bai and Ling Zhang and Rong Xiao and Mikael Elias and Sadowsky, {Michael J.} and Jingming Hu and Jorquera, {Milko A.}",

note = "Funding Information: 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.). Publisher Copyright: {\textcopyright} 2023, The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.",

year = "2023",

month = oct,

doi = "10.1007/s00248-023-02173-2",

language = "English (US)",

volume = "86",

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T1 - Structure and Functional Properties of Bacterial Communities in Surface Sediments of the Recently Declared Nutrient-Saturated Lake Villarrica in Southern Chile

AU - Campos, Marco A.

AU - Zhang, Qian

AU - Acuña, Jacquelinne J.

AU - Rilling, Joaquin I.

AU - Ruiz, Tay

AU - Carrazana, Elizabeth

AU - Reyno, Cristóbal

AU - Hollenback, Anthony

AU - Gray, Katelyn

AU - Jaisi, Deb P.

AU - Ogram, Andrew

AU - Bai, Junhong

AU - Zhang, Ling

AU - Xiao, Rong

AU - Elias, Mikael

AU - Sadowsky, Michael J.

AU - Hu, Jingming

AU - Jorquera, Milko A.

N1 - Funding Information: 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.). Publisher Copyright: © 2023, The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

PY - 2023/10

Y1 - 2023/10

N2 - 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.

AB - 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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KW - Bacterial diversity

KW - Community structure

KW - Functional genes

KW - Lake sediments

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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

Abstract

Bibliographical note

Keywords

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