Analysis of the bacteriorhodopsin-producing haloarchaea reveals a core community that is stable over time in the salt crystallizers of Eilat, Israel
Stability of microbial communities can impact the ability of dispersed cells to colonize a new habitat. Saturated brines and their halophile communities are presumed to be steady state systems due to limited environmental perturbations. In this study, the bacteriorhodopsin-containing fraction of the haloarchaeal community from Eilat salt crystallizer ponds was sampled five times over 3 years. Analyses revealed the existence of a constant core as several OTUs were found repeatedly over the length of the study: OTUs comprising 52 % of the total cloned and sequenced PCR amplicons were found in every sample, and OTUs comprising 89 % of the total sequences were found in more than one, and often more than two samples. LIBSHUFF and UNIFRAC analyses showed statistical similarity between samples and Spearman’s coefficient denoted significant correlations between OTU pairs, indicating non-random patterns in abundance and co-occurrence of detected OTUs. Further, changes in the detected OTUs were statistically linked to deviations in salinity. We interpret these results as indicating the existence of an ever-present core bacteriorhodopsin-containing Eilat crystallizer community that fluctuates in population densities, which are controlled by salinity rather than the extinction of some OTUs and their replacement through immigration and colonization.
KeywordsHaloarchaea Temporal analysis Seasonal Community stability Thalassohaline Eilat
The authors thank Salt of the Earth Eilat Ltd. for allowing access to the Eilat salterns; the Interuniversity Institute for Marine Sciences of Eilat for logistic support; the UConn Bioinformatics Facility for providing computing resources; and the reviewers for their invaluable comments. This research was supported by the National Science Foundation (award numbers, DEB0919290 and DEB0830024), the US-Israel Binational Science Foundation (Grant Number 2013061) and NASA Astrobiology: Exobiology and Evolutionary Biology Program Element (Grant Numbers NNX12AD70G and NNX15AM09G).
- Bidle K, Amadio W, Oliveira P, Paulish T, Hicks S, Earnest C (2005) Research article: a phylogenetic analysis of haloarchaea found in a solar saltern. BIOS 76:89–96. doi:10.1893/0005-3155(2005)076[0089:RAAPAO]2.0.CO;2Google Scholar
- Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Statist 11:265–270Google Scholar
- Dyall-Smith M (ed) (2008) The halohandbook: protocols for haloarchaeal genetics, 7 edn. http://www.haloarchaea.com/resources/halohandbook/index.html
- Fernández AB, Vera-Gargallo B, Sanchez-Porro C, Ghai R, Papke RT, Rodríguez-Valera F, Ventosa A (2014) Comparison of prokaryotic community structure from Mediterranean and Atlantic saltern concentrator ponds by a metagenomic approach. Front Microbiol 5:196. doi: 10.3389/fmicb.2014.00196 CrossRefPubMedPubMedCentralGoogle Scholar
- Legault BA, López-López A, Alba-Casado JC, Doolittle WF, Bolhuis H, Rodríguez-Valera F, Papke RT (2006) Environmental genomics of “Haloquadratum walsbyi” in a saltern crystallizer indicates a large pool of accessory genes in an otherwise coherent species. BMC Genom 7:171. doi: 10.1186/1471-2164-7-171 CrossRefGoogle Scholar
- Litchfield CD, Oren A, Irby A, Sikaroodi M, Gillevet PM (2009) Temporal and salinity impacts on the microbial diversity at the Eilat, Israel solar salt plant. Global NEST J 11:86–90Google Scholar
- Maddison D, Maddison W (2003) MacClade, 4.06 edn. Sinauer Associates, SunderlandGoogle Scholar
- Øvreås L, Daae FL, Torsvik V, Rodríguez-Valera F (2003) Characterization of microbial diversity in hypersaline environments by melting profiles and reassociation kinetics in combination with terminal restriction fragment length polymorphism (T-RFLP). Microb Ecol 46:291–301. doi: 10.1007/s00248-003-3006-3 CrossRefPubMedGoogle Scholar
- Stoeckenius W, Bivin D, McGinnis K (1985) Photoactive pigments in halobacteria from the Gavish Sabkha. In: Friedman G, Krumbein W (eds) Hypersaline ecosystems, vol 53. Ecological studies. Springer, Berlin Heidelberg, pp 288–295. doi: 10.1007/978-3-642-70290-7_16
- Tavaré S (1986) Some probablilistic and statistical problems in the anlysis of DNA sequences. In: Miura RM (ed) Some mathematical questions in biology. American Mathematical Society, ProvidenceGoogle Scholar
- Tukey JW (1977) Exploratory data analysis. Addison-Wesley Publishing Company, BostonGoogle Scholar