Longitudinal analysis of microbiota in microalga Nannochloropsis salina cultures

Geng, Haifeng; Sale, Kenneth L.; Tran-Gyamfi, Mary Bao; Lane, Todd W.; Yu, Eizadora T.

doi:10.1007/s00248-016-0746-4

Longitudinal analysis of microbiota in microalga Nannochloropsis salina cultures

Journal Article · Tue Mar 08 00:00:00 EST 2016 · Microbial Ecology

DOI:https://doi.org/10.1007/s00248-016-0746-4· OSTI ID:1343273

Geng, Haifeng ^[1]; Sale, Kenneth L. ^[1]; Tran-Gyamfi, Mary Bao ^[1]; Lane, Todd W. ^[1]; Yu, Eizadora T. ^[2]

Sandia National Lab. (SNL-CA), Livermore, CA (United States)
Sandia National Lab. (SNL-CA), Livermore, CA (United States); Univ. of the Philippines, Diliman Quezon City (Philippines)

Here, large-scale open microalgae cultivation has tremendous potential to make a significant contribution to replacing petroleum-based fuels with biofuels. Open algal cultures are unavoidably inhabited with a diversity of microbes that live on, influence, and shape the fate of these ecosystems. However, there is little understanding of the resilience and stability of the microbial communities in engineered semicontinuous algal systems. To evaluate the dynamics and resilience of the microbial communities in microalgae biofuel cultures, we conducted a longitudinal study on open systems to compare the temporal profiles of the microbiota from two multigenerational algal cohorts, which include one seeded with the microbiota from an in-house culture and the other exogenously seeded with a natural-occurring consortia of bacterial species harvested from the Pacific Ocean. From these month-long, semicontinuous open microalga Nannochloropsis salina cultures, we sequenced a time-series of 46 samples, yielding 8804 operational taxonomic units derived from 9,160,076 high-quality partial 16S rRNA sequences. We provide quantitative evidence that clearly illustrates the development of microbial community is associated with microbiota ancestry. In addition, N. salina growth phases were linked with distinct changes in microbial phylotypes. Alteromonadeles dominated the community in the N. salina exponential phase whereas Alphaproteobacteria and Flavobacteriia were more prevalent in the stationary phase. We also demonstrate that the N. salina-associated microbial community in open cultures is diverse, resilient, and dynamic in response to environmental perturbations. This knowledge has general implications for developing and testing design principles of cultivated algal systems.

View Accepted Manuscript (DOE)

Research Organization:: Sandia National Laboratories (SNL-CA), Livermore, CA (United States)

Sponsoring Organization:: Biological and Environmental Research (BER) (SC-23); Office of Science (SC); USDOE

Grant/Contract Number:: AC04-94AL85000

OSTI ID:: 1343273

Alternate ID(s):: OSTI ID: 1420901

Report Number(s):: SAND--2016-1584J; PII: 746

Journal Information:: Microbial Ecology, Journal Name: Microbial Ecology Journal Issue: 1 Vol. 72; ISSN 0095-3628

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

References (58)

Growth interactions between marine dinoflagellates in multispecies culture experiments Kayser, H. Marine Biology, Vol. 52, Issue 4 https://doi.org/10.1007/BF00389077	journal	January 1979
Growth interactions between marine dinoflagellates in multispecies culture experiments Kayser, H. Marine Biology, Vol. 52, Issue 4 https://doi.org/10.1007/bf00389077	journal	January 1979
Microbiome analysis of a microalgal mass culture growing in municipal wastewater in a prototype OMEGA photobioreactor Carney, Laura T.; Reinsch, Sigrid S.; Lane, Pamela D. Algal Research, Vol. 4 https://doi.org/10.1016/j.algal.2013.11.006	journal	April 2014
Eukaryotic and prokaryotic microbial communities during microalgal biomass production Lakaniemi, Aino-Maija; Hulatt, Chris J.; Wakeman, Kathryn D. Bioresource Technology, Vol. 124 https://doi.org/10.1016/j.biortech.2012.08.048	journal	November 2012
Biodiesel from algae: challenges and prospects Scott, Stuart A.; Davey, Matthew P.; Dennis, John S. Current Opinion in Biotechnology, Vol. 21, Issue 3 https://doi.org/10.1016/j.copbio.2010.03.005	journal	June 2010
Molecular mechanisms underlying roseobacter–phytoplankton symbioses Geng, Haifeng; Belas, Robert Current Opinion in Biotechnology, Vol. 21, Issue 3 https://doi.org/10.1016/j.copbio.2010.03.013	journal	June 2010
Synthetic ecology – A way forward for sustainable algal biofuel production? Kazamia, Elena; Aldridge, David C.; Smith, Alison G. Journal of Biotechnology, Vol. 162, Issue 1 https://doi.org/10.1016/j.jbiotec.2012.03.022	journal	November 2012
Marine microbial diversity: can it be determined? Pedrós-Alió, Carlos Trends in Microbiology, Vol. 14, Issue 6 https://doi.org/10.1016/j.tim.2006.04.007	journal	June 2006
Determination of nitrate in sea water by cadmium-copper reduction to nitrite Wood, E. D.; Armstrong, F. A. J.; Richards, F. A. Journal of the Marine Biological Association of the United Kingdom, Vol. 47, Issue 1 https://doi.org/10.1017/S002531540003352X	journal	February 1967
The diversity–stability debate McCann, Kevin Shear Nature, Vol. 405, Issue 6783 https://doi.org/10.1038/35012234	journal	May 2000
UniFrac: an effective distance metric for microbial community comparison Lozupone, Catherine; Lladser, Manuel E.; Knights, Dan The ISME Journal, Vol. 5, Issue 2 https://doi.org/10.1038/ismej.2010.133	journal	September 2010
The contribution of species richness and composition to bacterial services Bell, Thomas; Newman, Jonathan A.; Silverman, Bernard W. Nature, Vol. 436, Issue 7054 https://doi.org/10.1038/nature03891	journal	August 2005
Algae acquire vitamin B12 through a symbiotic relationship with bacteria Croft, Martin T.; Lawrence, Andrew D.; Raux-Deery, Evelyne Nature, Vol. 438, Issue 7064 https://doi.org/10.1038/nature04056	journal	November 2005
Initial community evenness favours functionality under selective stress Wittebolle, Lieven; Marzorati, Massimo; Clement, Lieven Nature, Vol. 458, Issue 7238 https://doi.org/10.1038/nature07840	journal	March 2009
Microbial community structure and its functional implications Fuhrman, Jed A. Nature, Vol. 459, Issue 7244 https://doi.org/10.1038/nature08058	journal	May 2009
Exploiting diversity and synthetic biology for the production of algal biofuels Georgianna, D. Ryan; Mayfield, Stephen P. Nature, Vol. 488, Issue 7411 https://doi.org/10.1038/nature11479	journal	August 2012
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Molecular eco-systems biology: towards an understanding of community function Raes, Jeroen; Bork, Peer Nature Reviews Microbiology, Vol. 6, Issue 9 https://doi.org/10.1038/nrmicro1935	journal	June 2008
Reductions in grassland species evenness increase dicot seedling invasion and spittle bug infestation Wilsey, Brian J.; Polley, H. Wayne Ecology Letters, Vol. 5, Issue 5 https://doi.org/10.1046/j.1461-0248.2002.00372.x	journal	September 2002
Bacterial community associated with Pfiesteria-like dinoflagellate cultures Alavi, Mohammad; Miller, Todd; Erlandson, Karn Environmental Microbiology, Vol. 3, Issue 6 https://doi.org/10.1046/j.1462-2920.2001.00207.x	journal	June 2001
Annually reoccurring bacterial communities are predictable from ocean conditions Fuhrman, J. A.; Hewson, I.; Schwalbach, M. S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 35 https://doi.org/10.1073/pnas.0602399103	journal	August 2006
Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism Amin, S. A.; Green, D. H.; Hart, M. C. Proceedings of the National Academy of Sciences, Vol. 106, Issue 40 https://doi.org/10.1073/pnas.0905512106	journal	September 2009
Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea McCarren, J.; Becker, J. W.; Repeta, D. J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 38 https://doi.org/10.1073/pnas.1010732107	journal	August 2010
Bacterial community structures are unique and resilient in full-scale bioenergy systems Werner, J. J.; Knights, D.; Garcia, M. L. Proceedings of the National Academy of Sciences, Vol. 108, Issue 10 https://doi.org/10.1073/pnas.1015676108	journal	February 2011
Meta-IDBA: a de Novo assembler for metagenomic data Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 27, Issue 13 https://doi.org/10.1093/bioinformatics/btr216	journal	June 2011
FragGeneScan: predicting genes in short and error-prone reads Rho, Mina; Tang, Haixu; Ye, Yuzhen Nucleic Acids Research, Vol. 38, Issue 20 https://doi.org/10.1093/nar/gkq747	journal	August 2010
A Broad Spectrum Artificial sea Water Medium for Coastal and open Ocean Phytoplankton1 Harrison, Paul J.; Waters, Rosemary E.; Taylor, F. J. R. Journal of Phycology, Vol. 16, Issue 1 https://doi.org/10.1111/j.0022-3646.1980.00028.x	journal	March 1980
Marine diatom species harbour distinct bacterial communities: Marine diatom species harbour distinct bacterial communities Grossart, Hans-Peter; Levold, Florian; Allgaier, Martin Environmental Microbiology, Vol. 7, Issue 6 https://doi.org/10.1111/j.1462-2920.2005.00759.x	journal	March 2005
Genomic content of uncultured Bacteroidetes from contrasting oceanic provinces in the North Atlantic Ocean: Genomic content of uncultivated marine Bacteroidetes Gómez-Pereira, Paola R.; Schüler, Margarete; Fuchs, Bernhard M. Environmental Microbiology, Vol. 14, Issue 1 https://doi.org/10.1111/j.1462-2920.2011.02555.x	journal	September 2011
Bacterial community transcription patterns during a marine phytoplankton bloom: Phytoplankton bloom metatranscriptome Rinta-Kanto, Johanna M.; Sun, Shulei; Sharma, Shalabh Environmental Microbiology, Vol. 14, Issue 1 https://doi.org/10.1111/j.1462-2920.2011.02602.x	journal	October 2011
Algicidal Bacteria in the Sea and their Impact on Algal Blooms1 Mayali, Xavier; Azam, Farooq The Journal of Eukaryotic Microbiology, Vol. 51, Issue 2 https://doi.org/10.1111/j.1550-7408.2004.tb00538.x	journal	March 2004
Microbial Population Structures in the Deep Marine Biosphere Huber, J. A.; Mark Welch, D. B.; Morrison, H. G. Science, Vol. 318, Issue 5847 https://doi.org/10.1126/science.1146689	journal	October 2007
Substrate-Controlled Succession of Marine Bacterioplankton Populations Induced by a Phytoplankton Bloom Teeling, H.; Fuchs, B. M.; Becher, D. Science, Vol. 336, Issue 6081 https://doi.org/10.1126/science.1218344	journal	May 2012
The Long-Term Stability of the Human Gut Microbiota Faith, Jeremiah J.; Guruge, Janaki L.; Charbonneau, Mark Science, Vol. 341, Issue 6141 https://doi.org/10.1126/science.1237439	journal	July 2013
Production of the Antimicrobial Secondary Metabolite Indigoidine Contributes to Competitive Surface Colonization by the Marine Roseobacter Phaeobacter sp. Strain Y4I Cude, W. Nathan; Mooney, Jason; Tavanaei, Arash A. Applied and Environmental Microbiology, Vol. 78, Issue 14 https://doi.org/10.1128/AEM.00297-12	journal	May 2012
Metagenome Survey of a Multispecies and Alga-Associated Biofilm Revealed Key Elements of Bacterial-Algal Interactions in Photobioreactors Krohn-Molt, Ines; Wemheuer, Bernd; Alawi, Malik Applied and Environmental Microbiology, Vol. 79, Issue 20 https://doi.org/10.1128/AEM.01641-13	journal	August 2013
Genetic Dissection of Tropodithietic Acid Biosynthesis by Marine Roseobacters Geng, H.; Bruhn, J. B.; Nielsen, K. F. Applied and Environmental Microbiology, Vol. 74, Issue 5 https://doi.org/10.1128/AEM.02339-07	journal	January 2008
Generation of Multimillion-Sequence 16S rRNA Gene Libraries from Complex Microbial Communities by Assembling Paired-End Illumina Reads Bartram, Andrea K.; Lynch, Michael D. J.; Stearns, Jennifer C. Applied and Environmental Microbiology, Vol. 77, Issue 11 https://doi.org/10.1128/AEM.02772-10	journal	April 2011
Differing Growth Responses of Major Phylogenetic Groups of Marine Bacteria to Natural Phytoplankton Blooms in the Western North Pacific Ocean Tada, Yuya; Taniguchi, Akito; Nagao, Ippei Applied and Environmental Microbiology, Vol. 77, Issue 12 https://doi.org/10.1128/AEM.02952-10	journal	April 2011
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB DeSantis, T. Z.; Hugenholtz, P.; Larsen, N. Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072 https://doi.org/10.1128/AEM.03006-05	journal	July 2006
Algicidal Effects of a Novel MarinePseudoalteromonas Isolate (Class Proteobacteria, Gamma Subdivision) on Harmful Algal Bloom Species of the GeneraChattonella, Gymnodinium, andHeterosigma Lovejoy, Connie; Bowman, John P.; Hallegraeff, Gustaaf M. Applied and Environmental Microbiology, Vol. 64, Issue 8 https://doi.org/10.1128/AEM.64.8.2806-2813.1998	journal	August 1998
Bacterial Community Structure Associated with a Dimethylsulfoniopropionate-Producing North Atlantic Algal Bloom Gonzalez, J. M.; Simo, R.; Massana, R. Applied and Environmental Microbiology, Vol. 66, Issue 10 https://doi.org/10.1128/AEM.66.10.4237-4246.2000	journal	October 2000
Involvement of an Extracellular Protease in Algicidal Activity of the Marine Bacterium Pseudoalteromonas sp. Strain A28 Lee, S. -o.; Kato, J.; Takiguchi, N. Applied and Environmental Microbiology, Vol. 66, Issue 10 https://doi.org/10.1128/AEM.66.10.4334-4339.2000	journal	October 2000
Parallel Processing of Substrate Correlates with Greater Functional Stability in Methanogenic Bioreactor Communities Perturbed by Glucose Hashsham, S. A.; Fernandez, A. S.; Dollhopf, S. L. Applied and Environmental Microbiology, Vol. 66, Issue 9 https://doi.org/10.1128/AEM.66.9.4050-4057.2000	journal	September 2000
Antibiotic Production by a Roseobacter Clade-Affiliated Species from the German Wadden Sea and Its Antagonistic Effects on Indigenous Isolates Brinkhoff, T.; Bach, G.; Heidorn, T. Applied and Environmental Microbiology, Vol. 70, Issue 4 https://doi.org/10.1128/AEM.70.4.2560-2565.2003	journal	April 2004
Overview of the Marine Roseobacter Lineage Buchan, A.; Gonzalez, J. M.; Moran, M. A. Applied and Environmental Microbiology, Vol. 71, Issue 10 https://doi.org/10.1128/AEM.71.10.5665-5677.2005	journal	October 2005
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities Lozupone, C.; Knight, R. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/AEM.71.12.8228-8235.2005	journal	December 2005
Expression of Tropodithietic Acid Biosynthesis Is Controlled by a Novel Autoinducer Geng, H.; Belas, R. Journal of Bacteriology, Vol. 192, Issue 17 https://doi.org/10.1128/JB.00410-10	journal	July 2010
Production of the Antimicrobial Secondary Metabolite Indigoidine Contributes to Competitive Surface Colonization by the Marine Roseobacter Phaeobacter sp. Strain Y4I Cude, W. Nathan; Mooney, Jason; Tavanaei, Arash A. Applied and Environmental Microbiology, Vol. 78, Issue 14 https://doi.org/10.1128/aem.00297-12	journal	May 2012
Metagenome Survey of a Multispecies and Alga-Associated Biofilm Revealed Key Elements of Bacterial-Algal Interactions in Photobioreactors Krohn-Molt, Ines; Wemheuer, Bernd; Alawi, Malik Applied and Environmental Microbiology, Vol. 79, Issue 20 https://doi.org/10.1128/aem.01641-13	journal	August 2013
Generation of Multimillion-Sequence 16S rRNA Gene Libraries from Complex Microbial Communities by Assembling Paired-End Illumina Reads Bartram, Andrea K.; Lynch, Michael D. J.; Stearns, Jennifer C. Applied and Environmental Microbiology, Vol. 77, Issue 11 https://doi.org/10.1128/aem.02772-10	journal	April 2011
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB DeSantis, T. Z.; Hugenholtz, P.; Larsen, N. Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072 https://doi.org/10.1128/aem.03006-05	journal	July 2006
Involvement of an Extracellular Protease in Algicidal Activity of the Marine Bacterium Pseudoalteromonas sp. Strain A28 Lee, S. -o.; Kato, J.; Takiguchi, N. Applied and Environmental Microbiology, Vol. 66, Issue 10 https://doi.org/10.1128/aem.66.10.4334-4339.2000	journal	October 2000
Environmental Biology of the Marine Roseobacter Lineage Wagner-Döbler, Irene; Biebl, Hanno Annual Review of Microbiology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.micro.60.080805.142115	journal	October 2006
Unlocking Short Read Sequencing for Metagenomics Rodrigue, Sébastien; Materna, Arne C.; Timberlake, Sonia C. PLoS ONE, Vol. 5, Issue 7 https://doi.org/10.1371/journal.pone.0011840	journal	July 2010
Interactions of the Algicidal Bacterium Kordia algicida with Diatoms: Regulated Protease Excretion for Specific Algal Lysis Paul, Carsten; Pohnert, Georg PLoS ONE, Vol. 6, Issue 6 https://doi.org/10.1371/journal.pone.0021032	journal	June 2011
Determination of Orthophosphate in Aqueous Solutions Containing Labile Organic and Inorganic Phosphorus Compounds1 Dick, W. A.; Tabatabai, M. A. Journal of Environment Quality, Vol. 6, Issue 1 https://doi.org/10.2134/jeq1977.00472425000600010018x	journal	January 1977
Identification of Carbohydrate Metabolism Genes in the Metagenome of a Marine Biofilm Community Shown to Be Dominated by Gammaproteobacteria and Bacteroidetes Edwards, Jennifer L.; Smith, Darren L.; Connolly, John Genes, Vol. 1, Issue 3 https://doi.org/10.3390/genes1030371	journal	October 2010

Cited By (2)

Changes in the Structure of the Microbial Community Associated with Nannochloropsis salina following Treatments with Antibiotics and Bioactive Compounds Geng, Haifeng; Tran-Gyamfi, Mary B.; Lane, Todd W. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01155	journal	July 2016
Analysis of microbiota in cultures of the green microalga Tetraselmis suecica Piampiano, Elisa; Pini, Francesco; Biondi, Natascia European Journal of Phycology, Vol. 54, Issue 3 https://doi.org/10.1080/09670262.2019.1606940	journal	April 2019

Similar Records

Changes in the Structure of the Microbial Community Associated with Nannochloropsis salina following Treatments with Antibiotics and Bioactive Compounds

Journal Article · Mon Jul 25 20:00:00 EDT 2016 · Frontiers in Microbiology · OSTI ID:1285957

Bacterial communities protect the alga Microchloropsis salina from grazing by the rotifer Brachionus plicatilis

Journal Article · Wed Apr 17 20:00:00 EDT 2019 · Algal Research · OSTI ID:1515196

Nuclear Genome Assembly of the Microalga Nannochloropsis salina CCMP1776

Journal Article · Wed Oct 30 20:00:00 EDT 2019 · Microbiology Resource Announcements · OSTI ID:1572429

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
algae
biosystem
microbiota
stability

Longitudinal analysis of microbiota in microalga Nannochloropsis salina cultures

Citation Formats

References (58)

Cited By (2)

Similar Records

Related Subjects