Abstract
Marine microbial communities experience daily fluctuations in light and temperature that can have important ramifications for carbon and nutrient cycling. Elucidation of such short time scale community-wide dynamics is hindered by system complexity. Hypersaline aquatic environments have lower species richness than marine environments and can be well-defined spatially, hence they provide a model system for diel cycle analysis. We conducted a 3-day time series experiment in a well-defined pool in hypersaline Lake Tyrrell, Australia. Microbial communities were tracked by combining cultivation-independent lipidomic, metagenomic and microscopy methods. The ratio of total bacterial to archaeal core lipids in the planktonic community increased by up to 58% during daylight hours and decreased by up to 32% overnight. However, total organism abundances remained relatively consistent over 3 days. Metagenomic analysis of the planktonic community composition, resolved at the genome level, showed dominance by Haloquadratum species and six uncultured members of the Halobacteriaceae. The post 0.8 μm filtrate contained six different nanohaloarchaeal types, three of which have not been identified previously, and cryo-transmission electron microscopy imaging confirmed the presence of small cells. Notably, these nano-sized archaea showed a strong diel cycle, with a pronounced increase in relative abundance over the night periods. We detected no eukaryotic algae or other photosynthetic primary producers, suggesting that carbon resources may derive from patchily distributed microbial mats at the sediment-water interface or from surrounding land. Results show the operation of a strong community-level diel cycle, probably driven by interconnected temperature, light abundance, dissolved oxygen concentration and nutrient flux effects.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Allen EE, Banfield JF . (2005). Community genomics in microbial ecology and evolution. Nat Rev Microbiol 3: 489–498.
Baker BJ, Banfield JF . (2003). Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44: 139–152.
Baliga NS . (2008). Systems biology - the scale of prediction. Science 320: 1297–1298.
Benjamini Y, Hochberg Y . (1995). Controlling the false discovery rate — a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57: 289–300.
Butte W . (1983). Rapid method for the determination of fatty-acid profiles from fats and oils using trimethylsulfonium hydroxiden for trans-esterification. J Chromatogr 261: 142–145.
Coker JA, DasSarma S . (2007). Genetic and transcriptomic analysis of transcription factor genes in the model halophilic Archaeon: coordinate action of TbpD and TfbA. BMC Genet 8: 61.
Comolli LR, Baker BJ, Downing KH, Siegerist CE, Banfield JF . (2009). Three-dimensional analysis of the structure and ecology of a novel, ultra-small archaeon. ISME J 3: 159–167.
Comolli LR, Duarte R, Baum D, Luef B, Downing KH, Larson DM et al. (2012). A portable cryo-plunger for on-site intact cryogenic microscopy sample preparation in natural environments. Microsc Res Tech 75: 829–836.
Comolli LR, Banfield JF . (2014). Inter-species interconnections in acid mine drainage microbial communities. Front Microbiol 5: 367.
Derosa M, Esposito E, Gambacorta A, Nicolaus B, Bulock JD . (1980). Effects of temperature on ether lipid-composition of Caldariella-Acidophila. Phytochemistry 19: 827–831.
Edgar RC . (2004a). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5: 1–19.
Edgar RC . (2004b). MUSCLE: multiple sequence alignment with improved accuracy and speed. 2004 IEEE Computational Systems Bioinformatics Conference, Proceedings. Stanford, CA, pp 728–729.
Emerson JB, Thomas BC, Andrade K, Allen EE, Heidelberg KB, Banfield JF . (2012). Dynamic viral populations in hypersaline systems as revealed by metagenomic assembly. Appl Environ Microb 78: 6309–6320.
Emerson JB, Andrade K, Thomas BC, Norman A, Allen EE, Heidelberg KB et al. (2013a). Virus-host and CRISPR dynamics in archaea-dominated hypersaline Lake Tyrrell, Victoria, Australia. Archaea 2013: 1–12.
Emerson JB, Thomas BC, Andrade K, Heidelberg KB, Banfield JF . (2013b). New approaches indicate constant viral diversity despite shifts in assemblage structure in an Australian hypersaline lake. Appl Environ Microb 79: 6755–6764.
Gasol JM, Casamayor EO, Joint I, Garde K, Gustavson K, Benlloch S et al. (2004). Control of heterotrophic prokaryotic abundance and growth rate in hypersaline planktonic environments. Aquat Microb Ecol 34: 193–206.
Ghai R, Pasic L, Fernandez AB, Martin-Cuadrado AB, Mizuno CM, McMahon KD et al. (2011). New abundant microbial groups in aquatic hypersaline environments. Sci Rep-Uk 1: 135.
Heidelberg KB, Nelson WC, Holm JB, Eisenkolb N, Andrade K, Emerson JB . (2013). Characterization of eukaryotic microbial diversity in hypersaline Lake Tyrrell, Australia. Front Microbiol 4: 115.
Herrmann AG, Knake D, Schneide. J, Peters H . (1973). Geochemistry of modern seawater and brines from salt pans - main components and bromine distribution. Contrib Mineral Petr 40: 1–24.
Hobbie JE, Daley RJ, Jasper S . (1977). Use of nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microb 33: 1225–1228.
Huang TC, Tu J, Chow TJ, Chen TH . (1990). Circadian-rhythm of the prokaryote Synechococcus Sp Rf-1. Plant Physiol 92: 531–533.
Huber H, Hohn MJ, Rachel R, Fuchs T, Wimmer VC, Stetter KO . (2002). A new phylum of archaea represented by a nanosized hyperthermophilic symbiont. Nature 417: 63–67.
Hug LA, Castelle CJ, Wrighton KC, Thomas BC, Sharon I, Frischkorn KR et al. (2013). Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling. Microbiome 1: 22.
Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ . (2010). Prodigal: prokaryotic gene recognition and translation initiation site identification. Bmc Bioinformatics 11: 119.
Johnson CH . (2005). Testing the adaptive value of circadian systems. Circadian Rhythms 393: 818–837.
Johnson CH, Mori T, Xu Y . (2008). A cyanobacterial circadian clockwork. Curr Biol 18: R816–R825.
Klinkhammer GP, Bender ML . (1980). The distribution of manganese in the Pacific-Ocean. Earth Planet Sc Lett 46: 361–384.
Langmead B, Trapnell C, Pop M, Salzberg SL . (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
Langmead B, Salzberg SL . (2012). Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359.
Lo I, Denef VJ, VerBerkmoes NC, Shah MB, Goltsman D, DiBartolo G et al. (2007). Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446: 537–541.
Macumber PG . (1992). Hydrological processes in the Tyrrell Basin, southeastern Australia. Chem Geol 96: 1–18.
Marr AG, Ingraham JL . (1962). Effect of temperature on composition of fatty acids in Escherichia Coli. J Bacteriol 84: 1260–126.
Miller CS, Baker BJ, Thomas BC, Singer SW, Banfield JF . (2011). EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data. Genome Biol 12: R44.
Mori T, Johnson CH . (2001). Independence of circadian timing from cell division in cyanobacteria. J Bacteriol 183: 2439–2444.
Narasingarao P, Podell S, Ugalde JA, Brochier-Armanet C, Emerson JB, Brocks JJ et al. (2012). De novo metagenomic assembly reveals abundant novel major lineage of archaea in hypersaline microbial communities. ISME J 6: 81–93.
Orellana MV, Pang WL, Durand PM, Whitehead K, Baliga NS . (2013). A role for programmed cell death in the microbial loop. Plos One 8: e6259.
Oren A . (2008). Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 4: 2.
Ottesen EA, Young CR, Eppley JM, Ryan JP, Chavez FP, Scholin CA et al. (2013). Pattern and synchrony of gene expression among sympatric marine microbial populations. Proc Natl Acad Sci USA 110: E488–E497.
Ottesen EA, Young CR, Gifford SM, Eppley JM, Marin R, Schuster SC et al. (2014). Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages. Science 345: 207–212.
Park JS, Kim HJ, Choi DH, Cho BC . (2003). Active flagellates grazing on prokaryotes in high salinity waters of a solar saltern. Aquat Microb Ecol 33: 173–179.
Pedros-Alio C, Calderon-Paz JI, MacLean MH, Medina G, Marrase C, Gasol JM et al. (2000). The microbial food web along salinity gradients. FEMS Microbiol Ecol 32: 143–155.
Peng Y, Leung HC, Yiu SM, Chin FY . (2012). IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics (Oxford, England) 28: 1420–1428.
Podar M, Makarova KS, Graham DE, Wolf YI, Koonin EV, Reysenbach AL . (2013). Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park. Biol Direct 8: 9.
Podell S, Ugalde JA, Narasingarao P, Banfield JF, Heidelberg KB, Allen EE . (2013). Assembly-driven community genomics of a hypersaline microbial ecosystem. Plos One 8: 1692.
Podell S, Emerson JB, Jones CM, Ugalde JA, Welch S, Heidelberg KB et al. (2014). Seasonal fluctuations in ionic concentrations drive microbial succession in a hypersaline lake community. ISME J 8: 979–990.
Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R et al. (2005). InterProScan: protein domains identifier. Nucleic Acids Res 33: W116–W120.
R_Core_Team. (2005). R: a language and environment for statistical computing In: Computing RFfS (ed).
Raes J, Bork P . (2008). Systems microbiology — timeline — molecular eco-systems biology: towards an understanding of community function. Nat Rev Microbiol 6: 693–699.
Ram RJ, VerBerkmoes NC, Thelen MP, Tyson GW, Baker BJ, Blake RC et al. (2005). Community proteomics of a natural microbial biofilm. Science 308: 1915–1920.
Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng JF et al. (2013). Insights into the phylogeny and coding potential of microbial dark matter. Nature 499: 431–437.
Rodriguez-Brito B, Li LL, Wegley L, Furlan M, Angly F, Breitbart M et al. (2010). Viral and microbial community dynamics in four aquatic environments. Isme Journal 4: 739–751.
Sorek R, Zhu YW, Creevey CJ, Francino MP, Bork P, Rubin EM . (2007). Genome-wide experimental determination of barriers to horizontal gene transfer. Science 318: 1449–1452.
Stamatakis A . (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics (Oxford, England) 22: 2688–2690.
Tagkopoulos I, Liu YC, Tavazoie S . (2008). Predictive behavior within microbial genetic networks. Science 320: 1313–1317.
Tsai AY, Gong GC, Sanders RW, Chiang KP, Huang JK, Chan YF . (2012). Viral lysis and nanoflagellate grazing as factors controlling diel variations of Synechococcus spp. summer abundance in coastal waters of Taiwan. Aquat Microb Ecol 66: 159–167.
Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM et al. (2004). Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428: 37–43.
Ugalde JA, Podell S, Narasingarao P, Allen EE . (2011). Xenorhodopsins, an enigmatic new class of microbial rhodopsins horizontally transferred between archaea and bacteria. Biol Direct 6: 52.
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 Microb 73: 5261–5267.
Whitehead K, Pan M, Masumura K, Bonneau R, Baliga NS . (2009). Diurnally entrained anticipatory behavior in archaea. Plos One 4: 5485.
Williams WD . (2001). Anthropogenic salinisation of inland waters. Hydrobiologia 466: 329–337.
Wilmes P, Bond PL . (2009). Microbial community proteomics: elucidating the catalysts and metabolic mechanisms that drive the Earth's biogeochemical cycles. Curr Opin Microbiol 12: 310–317.
Wu M, Eisen JA . (2008). A simple, fast, and accurate method of phylogenomic inference. Genome Biol 9: R151.
Acknowledgements
We thank Elizabeth Scott (USC) and Nadine Eisenkolb (USC) for fieldwork assistance. Funding for this work was provided by: NSF MCB Award #0626526 to JFB, EEA, and KBH. KA was supported by the ESPM Departmental Block grants, UC Berkeley Chancellors Fellowship, and the Andrew W Mellon Foundation fellowship. LRC was supported by the Director, Office of Science, Office of Basic Energy Sciences, of the US Department of Energy under contract no. DE-AC02-05CH11231. Cheetham Salt Works (Sea Lake, Australia) provided permission to collect samples.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Additional information
Supplementary Information accompanies this paper on The ISME Journal website
Supplementary information
Rights and permissions
About this article
Cite this article
Andrade, K., Logemann, J., Heidelberg, K. et al. Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem. ISME J 9, 2697–2711 (2015). https://doi.org/10.1038/ismej.2015.66
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2015.66
This article is cited by
-
Thrive or survive: prokaryotic life in hypersaline soils
Environmental Microbiome (2023)
-
Temperature-dependent expression of different guanine-plus-cytosine content 16S rRNA genes in Haloarcula strains of the class Halobacteria
Antonie van Leeuwenhoek (2019)
-
Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations
Nature Reviews Microbiology (2018)
-
Structure and diversity dynamics of microbial communities at day and night: investigation of meromictic Lake Doroninskoe, Transbaikalia, Russia
Journal of Oceanology and Limnology (2018)
