The microbial community in an alkaline saline sediment of a former maar lake bed
The “Hoya del Rincón de Parangueo (HRP)” is a maar that contained a perennial alkaline lake that drained in the 1980s so that a sediment with high pH and extreme salinity remained. The aim of this work was to determine how the bacterial and archaeal community was controlled by these extreme conditions.
Materials and methods
Sediment samples were collected from the 0–20-cm layer along a crater-wide transect. Physicochemical characteristics and the archaeal and bacterial community were determined by analysis of the 16S rRNA through Illumina sequencing.
Results and discussion
The sediment samples had a pH 10 and an electrolytic conductivity (EC) that ranged from 29.8 to 74.4 dS m−1. Three archaeal and 37 bacterial phyla were detected with Euryarchaeota (relative abundance 62.7 ± 17.6%) dominating the Archaea, and Proteobacteria (28.2 ± 10.7%) and Actinobacteria (21.1 ± 6.4%) the Bacteria. The most abundant archaeal genus was Candidatus Nitrososphaera while Euzebya, Halomonas, KSA1 and Planctomycetes dominated the bacterial gene. Thaumarchaeota were enriched in sediment samples with a higher Pb content and Euryarchaeota in sediment with a higher Mg content, while Crenarchaeota and Candidatus Nitrososphaera were enriched in sediment with a higher sand, total N and organic C content. Proteobacteria were enriched in sediment with a higher organic C and total N, Si and sand content, while Bacteroidetes and Planctomycetes in sediment with a higher water holding capacity and clay and Mg content. Members of KSA1 and Euzebya were enriched in sediment with a lower EC, organic C and total N content. Although a large number of bacterial and archaeal groups were correlated significantly with a range of sediment characteristics, the sediment characteristics explained the variation of only two bacterial groups > 50% (TM6 and Desulfonatronospira) using the machine learning tool randomForest and none of the archaeal groups. Archaeal and bacterial functional guilds were dominated by ammonium oxidation and nitrite reduction.
Although the different sediment samples were dominated often by similar bacterial and archaeal groups, the measured sediment characteristics explained little of the variation found between the sampling points. The high bacterial and archaeal diversity indicated that the site might be a source of unclassified species and phylotypes with specific metabolic capacities involved in the N and S cycles.
KeywordsAlpha diversity Diversity analysis Illumina sequencing Maar Microbial communities Transect
We thank Procuraduría Ambiental y de Ordenamiento Territorial del Estado de Guanajuato for access to the sampling site La Hoya del Rincón de Parangueo.
This research was funded by Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (Cinvestav-IPN, Mexico), and Apoyo Especial para Fortalecimiento de Doctorado PNPC 2013, 2014 and project Infraestructura 205945 from Consejo Nacional de Ciencia y Tecnología (CONACyT, Mexico) and project CB 2014-236674-Z from CONACyT. C.L. I.-S., and S. G.-A. received grant-aided support from CONACyT.
- Antranikian G, Suleiman M, Schäfers C, Adams MWW, Bartolucci S, Blamey JM, Birkeland NK, Bonch-Osmlovskaya E, da Costa MS, Cowan D, Danson M, Forterre P, Kelly R, Ishino Y, Littlechild J, Moracci M, Noll K, Oshima T, Robb F, Rossi M, Santos H, Schönheit P, Sterner R, Thauer R, Thomm M, Wiegel J, Stetter KO (2017) Diversity of Bacteria and Archaea from two shallow marine hydrothermal vents from Vulcano Island. Extremophiles 21:733–742CrossRefGoogle Scholar
- Aranda-Gómez JJ, Levresse G, Pacheco MJ, Ramos-Leal JA, Carrasco-Núñez G, Chacón-Baca E, González-Naranjo G, Chávez-Cabello G, Vega-González M, Origel G, Noyola-Medrano C (2013) Active sinking at the bottom of the Rincón de Parangueo maar (Guanajuato, México) and its probable relation with subsidence faults at Salamanca and Celaya. Bol la Soc Geol Mex 65:169–188Google Scholar
- Breiman L, Cutler A, (Fortran original) Liaw A, Wiener M (2018) Breiman and Cutler’s random forests for classification and regression. Package ‘randomForest’. Version: 4.6–14Google Scholar
- Bremner JM (1996) Nitrogen-Total. In: Sparks DL (ed) Methods of soil analysis: chemical methods Part 3. ASA, SSSA Madison, WI, pp 1085–1122Google Scholar
- Bryanskaya AV, Malup TK, Lazareva EV, Taran OP, Rozanov AS, Efimov VM, Peltek SE (2016) The role of environmental factors for the composition of microbial communities of saline lakes in the Novosibirsk region (Russia). BMC Microbiol 16. https://doi.org/10.1186/s12866-015-0618-y
- Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon J, Huttley GA, Kelley ST, Knights D, Koening JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010b) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefGoogle Scholar
- Cassel DK, Nielsen DR (1986) Field capacity and available water capacity. In: Klute A, Campbell GS, Jackson RD, Mortland MM, Nielsen DR (eds) Methods of soil analysis. Part, vol 1. Physical, mineralogical methods. ASA, SSSA, Madison, WI, pp 901–924Google Scholar
- Ceja-Navarro JA, Rivera-Orduña FN, Patiño-Zúñiga L, Villa-Sanjurjo A, Crossa J, Govaerts B, Dendooven L (2010) Phylogenetic and multivariate analyses to determine the effects of different tillage and residue management practices on soil bacterial communities. Appl Environ Microbiol 76:3685–3691CrossRefGoogle Scholar
- Compte-Port S, Borrego CM, Moussard H, Jeanbille M, Restrepo-Ortiz CX, de Diego A, Rodriguez-Iruretagoiena A, Gredilla A, Fdez-Ortiz de Vallejuelo S, Galand PE, Kalenitchenko D, Rols JL, Pokrovsky OS, Gonzalez AG, Camarero L, Muñiz S, Navarro-Navarro E, Auguet JC (2018) Metal contaminations impact archaeal community composition, abundance and function in remote alpine lakes. Environ Microbiol 20:2422–2437CrossRefGoogle Scholar
- Dojka MA, Hugenholtz P, Haack SK, Pace NR (1998) Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl Environ Microbiol 64:3869–3877Google Scholar
- Fernandez AB, Rasuk MC, Visscher PT, Contreras M, Novoa F, Poire DG, Patterson MM, Ventosa A, Farias ME (2016) Microbial diversity in sediment ecosystems (evaporites domes, microbial mats, and crusts) of hypersaline Laguna Tebenquiche, Salar de Atacama, Chile. Front Microbiol 7:1284CrossRefGoogle Scholar
- Gee GW, Bauder JW (1986) Particle size analysis. In: Klute A (ed) Methods of soil analysis, part, vol 1. physical and mineralogical Methods, ASA, SSSA, Madison, WI, pp 383–411Google Scholar
- Kienel U, Bowen SW, Byrne R, Park J, Böhnel H, Dulski P, Luhr JF, Siebert L, Huag GH, Negendank JFW (2009) First lacustrine varve chronologies from Mexico: impact of droughts, ENSO and human activity since AD 1840 as recorded in maar sediments from Valle de Santiago. J Paleolimnol 42:587–609CrossRefGoogle Scholar
- Kolde KR (2015) Maintainer Raivo, Package ‘pheatmap’, Version: 1.0.8Google Scholar
- Kuczynski J, Stombaugh J, Walters WA, González A, Caporaso JG, Knight R (2011) Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr Protoc Bioinformatics. https://doi.org/10.1002/0471250953.bi1007s36
- Kurahashi M, Fukunaga Y, Sakiyama Y, Harayama S, Yokota A (2010) Euzebya tangerine gen. nov., sp. nov., a deeply branching marine actinobacterium isolated from the sea Holothuria edulis, and proposal of Euzebyaceae ifam. nov., Euzebyales ord. nov. and Nitriliruptoridae subclassis nov. Int J Syst Evol Microbiol 60:2314–2319CrossRefGoogle Scholar
- Navarrete AA, Venturini AM, Meyer KM Klein AM, Tiedje JM, Bohannan BJ, Nüsslein K, Tsai SM, Rodrigues JL (2015) Differential response of Acidobacteria subgroups to forest-to-pasture conversion and their biogeographic patterns in the western Brazilian Amazon. Front Microbiol 6:1443CrossRefGoogle Scholar
- Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Vegan package in R. Community Ecology Package Version 2:4–3Google Scholar
- R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/.Google Scholar
- Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, PlainviewGoogle Scholar
- Spang A, Poehlein A, Offre P, Zumbrägel S, Haider S, Rychlik N, Nowka B, Schmeisser C, Lebedeva EV, Rattei T, Böhm C, Schmid M, Galushko A, Hatzenpichler R, Weinmaier T, Daniel R, Schleper C, Spieck E, Streit W, Wagner M (2012) The genome of the ammonia-oxidizing candidatus nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ Microbiol 14:3122–3145CrossRefGoogle Scholar
- Thomas GW (1996) Soil pH and soil acidity. In: Sparks DK (ed) Methods of soil analysis: chemical methods. Part, vol 3. ASA, SSSA, Madison, WI, pp 475–490Google Scholar
- USEPA (1996) “Method 3050B: acid digestion of sediments, sludges, and soils” revision 2. Washington, DCGoogle Scholar
- Valenzuela-Encinas C, Neria-González I, Alcántara-Hernández RJ, Enríquez-Aragón JA, Estrada-Alvarado I, Hernández-Rodríguez C, Dendooven L, Marsch R (2008) Phylogenetic analysis of the archaeal community in an alkaline-saline soil of the former lake Texcoco (Mexico). Extremophiles 12:247–254CrossRefGoogle Scholar
- Vuillemin A, Ariztegui D, Horn F, Kallmeyer J, Orsi WD, the PASADO Science Team (2018) Microbial community composition along a 50 000-year lacustrine sediment sequence. FEMS Microbiol Ecol 94. https://doi.org/10.1093/femsec/fiy029
- Wang NF, Zhang T, Yang X, Wang S, Yu Y, Dong LL, Guo YD, Ma YX, Zang JY (2016) Diversity and composition of bacterial community in soils and lake sediments from an arctic lake area. Front Microbiol 7:1170Google Scholar