Abstract
Purpose
Apart from having high concentrations of salt, some natural saline wetlands also go through cyclical fluctuations in water level. They are frequently considered vulnerable habitats. In the last decades, the reduction of rainfall in many areas, coupled with fertilizer overuse, is transforming wetlands, especially in climates with a pronounced dry season. We studied a seasonally flooded saline wetland, and focused on the changes in the microbial communities.
Methods
High-throughput sequencing was used to explore the diversity and structure of the prokaryotic communities present in the surface sediments. A water and soil salinity gradient along different lagoons in the wetland complex was observed.
Results
Salinity affected both microbial richness and composition. The highest microbial richness was observed in lagoons with lower salinity. Statistical analysis suggests that the differences in community composition were associated with differences in salinity level, although an anthropic disturbance (increasing levels of soil organic matter, SOM) that was present predominantly in one lagoon also had a noticeable effect. Sorting of samples using beta diversity distances revealed that differences among communities were due to the distinct habitats, that is, a lagoon’s salinity and SOM, not water level cycles. Differences between flooded and dry-out seasons were also explored and the linear model showed that only a small number of OTUs (2.5%) had statistical differences between seasons.
Conclusion
Our findings will help in understanding the effects that both salinity and drying-out periods, which are increasing problems worldwide, may have on microbial communities and their resistance to seasonal fluctuations in water levels.
This is a preview of subscription content, log in via an institution to check access.
References
Abdallah MB, Karray F, Mhiri N et al (2016) Prokaryotic diversity in a Tunisian hypersaline lake, Chott El Jerid. Extremophiles 20:125–138. https://doi.org/10.1007/s00792-015-0805-7
Alonso M (2002) Humedales. In: Reyero JM (ed) La Naturaleza en España. Ministerio de Medio Ambiente, Madrid, pp 110–127
An J, Liu C, Wang Q et al (2019) Soil bacterial community structure in Chinese wetlands. Geoderma 337:290–299. https://doi.org/10.1016/j.geoderma.2018.09.035
Arroyo P, Sáenz de Miera LE, Ansola G (2015) Influence of environmental variables on the structure and composition of soil bacterial communities in natural and constructed wetlands. Sci Total Environ 506–507:380–390. https://doi.org/10.1016/j.scitotenv.2014.11.039
Bachran M, Kluge S, Lopez-Fernandez M, Cherkouk A (2019) Microbial diversity in an arid, naturally saline environment. Microb Ecol 78:494–505. https://doi.org/10.1007/s00248-018-1301-2
Behera P, Mahapatra S, Mohapatra M et al (2017) Salinity and macrophyte drive the biogeography of the sedimentary bacterial communities in a brackish water tropical coastal lagoon. Sci Total Environ 595:472–485. https://doi.org/10.1016/j.scitotenv.2017.03.271
Bender EA, Case TJ, Gilpin ME (1984) Perturbation experiments in community ecology : theory and practice. Ecology 65:1–13. https://doi.org/10.2307/1939452
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300
Berga M, Zha Y, Székely AJ, Langenheder S (2017) Functional and compositional stability of bacterial metacommunities in response to salinity changes. Front Microbiol 8:1–11. https://doi.org/10.3389/fmicb.2017.00948
Boujelben I, Martínez-García M, van Pelt J, Maalej S (2014) Diversity of cultivable halophilic archaea and bacteria from superficial hypersaline sediments of Tunisian solar salterns. Antonie Van Leeuwenhoek, Int J Gen Mol Microbiol 106:675–692. https://doi.org/10.1007/s10482-014-0238-9
Bradshaw DJ, Dickens NJ, Trefry JH, McCarthy PJ (2020) Defining the sediment prokaryotic communities of the Indian river lagoon, FL, USA, an estuary of national significance. PLoS ONE 15:1–24. https://doi.org/10.1371/journal.pone.0236305
Camacho C, Coulouris G, Avagyan V et al (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:1–9. https://doi.org/10.1186/1471-2105-10-421
Canfora L, Bacci G, Pinzari F et al (2014) Salinity and bacterial diversity: to what extent does the concentration of salt affect the bacterial community in a saline soil? PLoS ONE 9:e106662. https://doi.org/10.1371/journal.pone.0106662
Caporaso JG, Lauber CL, Walters WA et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108:4516–4522. https://doi.org/10.1073/pnas.1000080107
Caporaso JG, Lauber CL, Walters WA et al (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. https://doi.org/10.1038/ismej.2012.8
Casamayor EO, Triadó-Margarit X, Castañeda C (2013) Microbial biodiversity in saline shallow lakes of the Monegros desert, Spain. FEMS Microbiol Ecol 85:503–518. https://doi.org/10.1111/1574-6941.12139
Chen S, Liu X, Dong X (2005) Syntrophobacter sulfatireducens sp. nov., a novel syntrophic, propionate-oxidizing bacterium isolated from UASB reactors. Int J Syst Evol Microbiol 55:1319–1324. https://doi.org/10.1099/ijs.0.63565-0
Çınar S, Mutlu MB (2016) Comparative analysis of prokaryotic diversity in solar salterns in eastern Anatolia (Turkey). Extremophiles 20:589–601. https://doi.org/10.1007/s00792-016-0845-7
Cole JR, Wang Q, Fish JA et al (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:633–642. https://doi.org/10.1093/nar/gkt1244
Dungan RS, Leytem AB (2015) Detection of purple sulfur bacteria in purple and non-purple dairy wastewaters. J Environ Qual 44:1550–1555. https://doi.org/10.2134/jeq2015.03.0128
Fernández AB, Ghai R, Martin-Cuadrado AB et al (2014) Prokaryotic taxonomic and metabolic diversity of an intermediate salinity hypersaline habitat assessed by metagenomics. FEMS Microbiol Ecol 88:623–635. https://doi.org/10.1111/1574-6941.12329
Guerra-Doce E, Abarquero-Moras FJ, Delibes-de-Castro G, et al (2012) Salt production at the Villafáfila lake complex (Zamora, Spain) in prehistoric times. In: Bacvarov VNK, Tarnovo VFV (eds) Salt and gold: the role of salt in prehistoric Europe. Alexander von Humboldt Foundation, Bonn, Germany, p 360
Haferburg G, Gröning JAD, Schmidt N et al (2017) Microbial diversity of the hypersaline and lithium-rich Salar de Uyuni, Bolivia. Microbiol Res 199:19–28. https://doi.org/10.1016/j.micres.2017.02.007
Han R, Zhang X, Liu J et al (2017) Microbial community structure and diversity within hypersaline Keke salt lake environments. Can J Microbiol 63:895–908. https://doi.org/10.1139/cjm-2016-0773
Herlemann DPR, Labrenz M, Jürgens K et al (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic sea. ISME J 5:1571–1579. https://doi.org/10.1038/ismej.2011.41
Herrero J, Weindorf DC, Castañeda C (2015) Two fixed ratio dilutions for soil salinity monitoring in hypersaline wetlands. PLoS ONE 10:1–18. https://doi.org/10.1371/journal.pone.0126493
Hollister EB, Engledow AS, Hammett AJM et al (2010) Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments. ISME J 4:829–838. https://doi.org/10.1038/ismej.2010.3
Holmes DE, Nevin KP, Woodard TL et al (2007) Prolixibacter bellariivorans gen. nov., sp. nov., a sugar-fermenting, psychrotolerant anaerobe of the phylum Bacteroidetes, isolated from a marine-sediment fuel cell. Int J Syst Evol Microbiol 57:701–707. https://doi.org/10.1099/ijs.0.64296-0
Ikenaga M, Guevara R, Dean AL et al (2010) Changes in community structure of sediment bacteria along the florida coastal everglades marsh-mangrove-seagrass salinity gradient. Microb Ecol 59:284–295. https://doi.org/10.1007/s00248-009-9572-2
Jin X, Ma Y, Kong Z et al (2019) The variation of sediment bacterial community in response to anthropogenic disturbances of Poyang lake, China. Wetlands 39:63–73. https://doi.org/10.1007/s13157-017-0909-1
Kirchman DL (2002) The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39:91–100. https://doi.org/10.1016/S0168-6496(01)00206-9
Kumar S, Stecher G, Tamura T (2015) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 1–11. https://doi.org/10.1093/molbev/msw054
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmer test package: tests in linear mixed effects models. J Stat Softw 82:26. https://doi.org/10.18637/jss.v082.i13
Liu P, Bai J, Ding Q et al (2012) Effects of water level and salinity on TN and TP contents in marsh soils of the Yellow river delta, China. Clean - Soil, Air, Water 40:1118–1124. https://doi.org/10.1002/clen.201200029
Liu Y, Sui X, Li F, et al (2018) Effects of various interference intensities on the soil bacterial communities diversity in the Sanjiang plain, northeast China. Int J Agric Biol 20:695–700. https://doi.org/10.17957/IJAB/15.0563
Losey NA, Stevenson BS, Busse HJ et al (2013) Thermoanaerobaculum aquaticum gen. nov., sp. nov., the first cultivated member of acidobacteria subdivision 23, isolated from a hot spring. Int J Syst Evol Microbiol 63:4149–4157. https://doi.org/10.1099/ijs.0.051425-0
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005
Ma B, Gong J (2013) A meta-analysis of the publicly available bacterial and archaeal sequence diversity in saline soils. World J Microbiol Biotechnol 29:2325–2334. https://doi.org/10.1007/s11274-013-1399-9
Nawrocki EP, Kolbe DL, Eddy SR (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25:1335–1337. https://doi.org/10.1093/bioinformatics/btp157
Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. In: Bigham JM (ed) Methods of soil analysis Part3 chemical methods. Soil Science Society of America, Inc., American Society of Agronomy Inc, Madison, Wisconsin, USA, pp 961–1010
Núñez Salazar R, Aguirre C, Soto J et al (2020) Physicochemical parameters affecting the distribution and diversity of the water column microbial community in the high-altitude andean lake system of La Brava and La Punta. Microorganisms 8:1–24. https://doi.org/10.3390/microorganisms8081181
Oksanen J, Blanchet FG, Kindt R, et al (2010) Vegan: community ecology package. R package version 1.17-4. 2010
Peralta RM, Ahn C, Gillevet PM (2013) Characterization of soil bacterial community structure and physicochemical properties in created and natural wetlands. Sci Total Environ 443:725–732. https://doi.org/10.1016/j.scitotenv.2012.11.052
Price MN, Dehal PS, Arkin AP (2010) FastTree 2 - Approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. https://doi.org/10.1371/journal.pone.0009490
Rathour R, Gupta J, Mishra A et al (2020) A comparative metagenomic study reveals microbial diversity and their role in the biogeochemical cycling of Pangong lake. Sci Total Environ 731:139074. https://doi.org/10.1016/j.scitotenv.2020.139074
R Core Team (2018). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rengasamy P (2006) World salinization with emphasis on Australia. J Exp Bot 57:1017–1023. https://doi.org/10.1093/jxb/erj108
Rognes T, Flouri T, Nichols B et al (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 2016:1–22. https://doi.org/10.7717/peerj.2584
Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
Sims A, Zhang Y, Gajaraj S et al (2013) Toward the development of microbial indicators for wetland assessment. Water Res 47:1711–1725. https://doi.org/10.1016/j.watres.2013.01.023
Sousa WP (1984) The role of disturbance in natural communities. Ann Rev Ecol Syst 15:353–391
Tang X, Xie G, Shao K et al (2012) Influence of salinity on the bacterial community composition in lake Bosten, a large oligosaline lake in arid northwestern China. Appl Environ Microbiol 78:4748–4751. https://doi.org/10.1128/AEM.07806-11
Thomas GW (1996) Soil pH and soil acidity. In: Bigham JM (ed) Methods of soil analysis part3 chemical methods. Soil Science Society of America, Inc., American Society of Agronomy Inc, Madison, Wisconsin, USA, pp 475–490
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07
Widdel F, Pfennig N (1982) Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids II. Incomplete oxidation of propionate by Desulfobulbus propionicus gen. nov., sp. nov. Arch Microbiol 131:360–365
Wu Y, Tam NFY, Wong MH (2008) Effects of salinity on treatment of municipal wastewater by constructed mangrove wetland microcosms. Mar Pollut Bull 57:727–734. https://doi.org/10.1016/j.marpolbul.2008.02.026
Xiong J, Liu Y, Lin X et al (2012) Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ Microbiol 14:2457–2466. https://doi.org/10.1111/j.1462-2920.2012.02799.x
Yamada T, Sekiguchi Y, Hanada S et al (2006) Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the. Int J Syst Evol Microbiol 56:1331–1340. https://doi.org/10.1099/ijs.0.64169-0
Yang J, Ma L, Jiang H et al (2016) Salinity shapes microbial diversity and community structure in surface sediments of the Qinghai-Tibetan lakes. Sci Rep 6:6–11. https://doi.org/10.1038/srep25078
Yergeau E, Michel C, Tremblay J et al (2017) Metagenomic survey of the taxonomic and functional microbial communities of seawater and sea ice from the Canadian Arctic. Sci Rep 7:1–10. https://doi.org/10.1038/srep42242
Zhu D, Han R, Long Q et al (2020) An evaluation of the core bacterial communities associated with hypersaline environments in the Qaidam basin, China. Arch Microbiol 202:2093–2103. https://doi.org/10.1007/s00203-020-01927-7
Acknowledgements
We want to thank Mariano Rodríguez, director of the “Reserva Natural de Las Lagunas de Villafáfila,” for all his collaboration and assistance.
Author information
Authors and Affiliations
Contributions
All authors have contributed significantly to the project and merit to be included as co-authors.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible editor: Terrence H. Bell
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
11368_2021_3026_MOESM1_ESM.xlsx
Supplementary file1 Supplementary Table S1. Description of the linear models used in the analysis to test the effect of lagoon and water level factors, as well as their interaction. Description of mixed models used to explore the water level factor, considering sample localization as a random effect. Response variables analyzed with these models included: Phsyco-Chemical parameters; indexes of alpha diversity; position of communities on the first three axes of the PCoAs for the two estimated distances; and logarithm of the relative abundance of each OTU. Significant P-values are in light salmon, and those with P < 10–6 are in dark salmon color. Samples grouped by lagoon and water level stage (season) are depicted using a color gradient in magenta. The names of species with OTUs that have more than 90% identity with NCBI’s RefSeq 16S databases are also shown. (PDF 2.11 MB)
11368_2021_3026_MOESM2_ESM.pdf
Supplementary file2 Supplementary Figure S1. Boxplots showing relative abundance of certain taxa for the salty and the non-salty lagoons. Abundance represented as the logs of normalized reads. Different patterns among lagoons can be appreciated. See text for a more detailed explanation. (PDF 18 KB)
11368_2021_3026_MOESM3_ESM.pdf
Supplementary file3 Supplementary Figure S2. Boxplots of taxonomically far distanced taxa, with higher frequency during the flooded stage (F) or dried-out stage (D). Abundance represented as the logs of normalized reads. Taxa more frequent in F were Deltaproteobacteria, Bacteroidia, and Planctomycetaceae; while in D were: Actinobacteria, Cytophagia, and Group 21 of Acidobacteria. (PDF 16 KB)
Rights and permissions
About this article
Cite this article
Sáenz de Miera, L.E., Gutiérrez-González, J.J., Arroyo, P. et al. Prokaryotic community diversity in the sediments of saline lagoons and its resistance to seasonal disturbances by water level cycles. J Soils Sediments 21, 3169–3184 (2021). https://doi.org/10.1007/s11368-021-03026-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-021-03026-6