Modified niche optima and breadths explain the historical contingency of bacterial community responses to eutrophication in coastal sediments
Abstract
Abstract Previous studies have shown that the response of bacterial communities to disturbances depends on their environmental history. Historically fluctuating habitats host communities that respond better to disturbance than communities of historically stable habitats. However, the exact ecological mechanism that drives this dependency remains unknown. Here, we experimentally demonstrate that modifications of niche optima and niche breadths of the community members are driving this dependency of bacterial responses to past environmental conditions. First, we develop a novel, simple method to calculate the niche optima and breadths of bacterial taxa regarding single environmental gradients. Then, we test this method on sediment bacterial communities of three habitats, one historically stable and less loaded and two historically more variable and more loaded habitats in terms of historical chlorophyll‐α water concentration, that we subject to hypoxia via organic matter addition ex situ . We find that communities containing bacterial taxa differently adapted to hypoxia show different structural and functional responses, depending on the sediment's environmental history. Specifically, in the historically less fluctuating and loaded sediments where we find more taxa poorly adapted to hypoxic conditions, communities change a lot over time and organic matter is not degraded efficiently. The opposite is true for themore »
- Authors:
-
- Biological and Environmental Sciences and Engineering Department King Abdullah University of Science and Technology (KAUST) Thuwal 23955‐6900 Saudi Arabia, Department of Biology University of Crete Voutes University Campus 70013 Heraklion Crete Greece
- School of Biological and Chemical Sciences Queen Mary University of London Mile End Road London E1 4NS UK
- Department of Biology University of Crete Voutes University Campus 70013 Heraklion Crete Greece
- Biological and Environmental Sciences and Engineering Department King Abdullah University of Science and Technology (KAUST) Thuwal 23955‐6900 Saudi Arabia
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1328803
- Alternate Identifier(s):
- OSTI ID: 1328804
- Grant/Contract Number:
- DE‐AC02‐05CH11231; AC02-05CH11231
- Resource Type:
- Journal Article: Published Article
- Journal Name:
- Molecular Ecology
- Additional Journal Information:
- Journal Name: Molecular Ecology Journal Volume: 26 Journal Issue: 7; Journal ID: ISSN 0962-1083
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Fodelianakis, S., Moustakas, A., Papageorgiou, N., Manoli, O., Tsikopoulou, I., Michoud, G., Daffonchio, D., Karakassis, I., and Ladoukakis, E. D. Modified niche optima and breadths explain the historical contingency of bacterial community responses to eutrophication in coastal sediments. United Kingdom: N. p., 2016.
Web. doi:10.1111/mec.13842.
Fodelianakis, S., Moustakas, A., Papageorgiou, N., Manoli, O., Tsikopoulou, I., Michoud, G., Daffonchio, D., Karakassis, I., & Ladoukakis, E. D. Modified niche optima and breadths explain the historical contingency of bacterial community responses to eutrophication in coastal sediments. United Kingdom. https://doi.org/10.1111/mec.13842
Fodelianakis, S., Moustakas, A., Papageorgiou, N., Manoli, O., Tsikopoulou, I., Michoud, G., Daffonchio, D., Karakassis, I., and Ladoukakis, E. D. 2016.
"Modified niche optima and breadths explain the historical contingency of bacterial community responses to eutrophication in coastal sediments". United Kingdom. https://doi.org/10.1111/mec.13842.
@article{osti_1328803,
title = {Modified niche optima and breadths explain the historical contingency of bacterial community responses to eutrophication in coastal sediments},
author = {Fodelianakis, S. and Moustakas, A. and Papageorgiou, N. and Manoli, O. and Tsikopoulou, I. and Michoud, G. and Daffonchio, D. and Karakassis, I. and Ladoukakis, E. D.},
abstractNote = {Abstract Previous studies have shown that the response of bacterial communities to disturbances depends on their environmental history. Historically fluctuating habitats host communities that respond better to disturbance than communities of historically stable habitats. However, the exact ecological mechanism that drives this dependency remains unknown. Here, we experimentally demonstrate that modifications of niche optima and niche breadths of the community members are driving this dependency of bacterial responses to past environmental conditions. First, we develop a novel, simple method to calculate the niche optima and breadths of bacterial taxa regarding single environmental gradients. Then, we test this method on sediment bacterial communities of three habitats, one historically stable and less loaded and two historically more variable and more loaded habitats in terms of historical chlorophyll‐α water concentration, that we subject to hypoxia via organic matter addition ex situ . We find that communities containing bacterial taxa differently adapted to hypoxia show different structural and functional responses, depending on the sediment's environmental history. Specifically, in the historically less fluctuating and loaded sediments where we find more taxa poorly adapted to hypoxic conditions, communities change a lot over time and organic matter is not degraded efficiently. The opposite is true for the historically more fluctuating and loaded sediments where we find more taxa well adapted to hypoxia. Based on the community responses observed here, we also propose an alternative calculation of community resistance that takes into account how rapidly the communities respond to disturbances and not just the initial and final states of the community.},
doi = {10.1111/mec.13842},
url = {https://www.osti.gov/biblio/1328803},
journal = {Molecular Ecology},
issn = {0962-1083},
number = 7,
volume = 26,
place = {United Kingdom},
year = {Fri Oct 07 00:00:00 EDT 2016},
month = {Fri Oct 07 00:00:00 EDT 2016}
}
Web of Science
Works referenced in this record:
Eutrophication of Chesapeake Bay: historical trends and ecological interactions
journal, November 2005
- Kemp, Wm; Boynton, Wr; Adolf, Je
- Marine Ecology Progress Series, Vol. 303
Prokaryotes: The unseen majority
journal, June 1998
- Whitman, W. B.; Coleman, D. C.; Wiebe, W. J.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 12
Beyond biogeographic patterns: processes shaping the microbial landscape
journal, May 2012
- Hanson, China A.; Fuhrman, Jed A.; Horner-Devine, M. Claire
- Nature Reviews Microbiology, Vol. 10, Issue 7
Microbial diversity in the deep sea and the underexplored "rare biosphere"
journal, July 2006
- Sogin, M. L.; Morrison, H. G.; Huber, J. A.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 32
Local and regional factors influencing bacterial community assembly: Bacterial community assembly
journal, April 2011
- Lindström, Eva S.; Langenheder, Silke
- Environmental Microbiology Reports, Vol. 4, Issue 1
Differences in structure and dynamics of Polynucleobacter communities in a temperate and a subtropical lake, revealed at three phylogenetic levels: Structure and dynamics of Polynucleobacter communities
journal, July 2006
- Wu, Qinglong L.; Hahn, Martin W.
- FEMS Microbiology Ecology, Vol. 57, Issue 1
Fundamentals of Microbial Community Resistance and Resilience
journal, January 2012
- Shade, Ashley; Peter, Hannes; Allison, Steven D.
- Frontiers in Microbiology, Vol. 3
Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences
journal, August 2013
- Langille, Morgan G. I.; Zaneveld, Jesse; Caporaso, J. Gregory
- Nature Biotechnology, Vol. 31, Issue 9
Drift in ocean currents impacts intergenerational microbial exposure to temperature
journal, May 2016
- Doblin, Martina A.; van Sebille, Erik
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 20
Hydrologic history influences microbial community composition and nitrogen cycling under experimental drying/wetting treatments
journal, November 2013
- Peralta, Ariane L.; Ludmer, Sarah; Kent, Angela D.
- Soil Biology and Biochemistry, Vol. 66
Quantification of macrobenthic effects on diagenesis using a multicomponent inverse model in salt marsh sediments
journal, November 2004
- Furukawa, Yoko; Smith, April C.; Kostka, Joel E.
- Limnology and Oceanography, Vol. 49, Issue 6
Mass wasting and uplift on Crete and Karpathos during the early Pliocene related to initiation of south Aegean left-lateral, strike-slip tectonics
journal, July 2008
- Zachariasse, W. J.; van Hinsbergen, D. J. J.; Fortuin, A. R.
- Geological Society of America Bulletin, Vol. 120, Issue 7-8
Levels and limits in artificial selection of communities
journal, August 2015
- Blouin, Manuel; Karimi, Battle; Mathieu, Jérôme
- Ecology Letters, Vol. 18, Issue 10
Temporal variation of β-diversity and assembly mechanisms in a bacterial metacommunity
journal, December 2011
- Langenheder, Silke; Berga, Mercè; Östman, Örjan
- The ISME Journal, Vol. 6, Issue 6
Microbiomes in light of traits: A phylogenetic perspective
journal, November 2015
- Martiny, J. B. H.; Jones, S. E.; Lennon, J. T.
- Science, Vol. 350, Issue 6261
Coexistence of Specialist and Generalist Species Is Shaped by Dispersal and Environmental Factors
journal, May 2014
- Büchi, Lucie; Vuilleumier, Séverine
- The American Naturalist, Vol. 183, Issue 5
Tolerance of riverine plants to flooding and exposure indicated by water regime
journal, January 1999
- Blanch, Stuart J.; Ganf, George G.; Walker, Keith F.
- Regulated Rivers: Research & Management, Vol. 15, Issue 1-3
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
journal, June 2010
- Caporaso, J. G.; Lauber, C. L.; Walters, W. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
Assessing the biodegradability of terrestrially-derived organic matter in Scottish sea loch sediments
journal, January 2008
- Loh, P. S.; Miller, A. E. J.; Reeves, A. D.
- Hydrology and Earth System Sciences, Vol. 12, Issue 3
Bacterial community response to changes in soil redox potential along a moisture gradient in restored wetlands
journal, December 2014
- Peralta, Ariane L.; Ludmer, Sarah; Matthews, Jeffrey W.
- Ecological Engineering, Vol. 73
Conceptual Synthesis in Community Ecology
journal, June 2010
- Vellend, Mark
- The Quarterly Review of Biology, Vol. 85, Issue 2
Mapping the niche space of soil microorganisms using taxonomy and traits
journal, August 2012
- Lennon, Jay T.; Aanderud, Zachary T.; Lehmkuhl, B. K.
- Ecology, Vol. 93, Issue 8
Patterns and Processes of Microbial Community Assembly
journal, September 2013
- Nemergut, D. R.; Schmidt, S. K.; Fukami, T.
- Microbiology and Molecular Biology Reviews, Vol. 77, Issue 3
The role of Environmental and Spatial Factors for the Composition of Aquatic Bacterial Communities
journal, September 2007
- Langenheder, Silke; Ragnarsson, Henrik
- Ecology, Vol. 88, Issue 9
The Western English Channel contains a persistent microbial seed bank
journal, November 2011
- Caporaso, J. Gregory; Paszkiewicz, Konrad; Field, Dawn
- The ISME Journal, Vol. 6, Issue 6
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
Sulfur, carbon, and nitrogen cycling in faunated marine sediments impacted by repeated organic enrichment
journal, February 2010
- Valdemarsen, T.; Kristensen, E.; Holmer, M.
- Marine Ecology Progress Series, Vol. 400
Resilience vs. historical contingency in microbial responses to environmental change
journal, May 2015
- Hawkes, Christine V.; Keitt, Timothy H.
- Ecology Letters, Vol. 18, Issue 7
Chlorophyll a algorithms for oligotrophic oceans: A novel approach based on three-band reflectance difference : A NOVEL OCEAN CHLOROPHYLL
journal, January 2012
- Hu, Chuanmin; Lee, Zhongping; Franz, Bryan
- Journal of Geophysical Research: Oceans, Vol. 117, Issue C1
Bacterial taxa-area and distance-decay relationships in marine environments
journal, January 2014
- Zinger, L.; Boetius, A.; Ramette, A.
- Molecular Ecology, Vol. 23, Issue 4
Engineering Microbiomes to Improve Plant and Animal Health
journal, October 2015
- Mueller, U. G.; Sachs, J. L.
- Trends in Microbiology, Vol. 23, Issue 10
Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought
journal, November 2012
- Bouskill, Nicholas J.; Lim, Hsiao Chien; Borglin, Sharon
- The ISME Journal, Vol. 7, Issue 2
Insight into biases and sequencing errors for amplicon sequencing with the Illumina MiSeq platform
journal, January 2015
- Schirmer, Melanie; Ijaz, Umer Z.; D'Amore, Rosalinda
- Nucleic Acids Research, Vol. 43, Issue 6
A social–ecological framework for “micromanaging” microbial services
journal, November 2014
- Peralta, Ariane L.; Stuart, Diana; Kent, Angela D.
- Frontiers in Ecology and the Environment, Vol. 12, Issue 9
Is dispersal limitation more prevalent in the ocean?
journal, January 2013
- Srivastava, Diane S.; Kratina, Pavel
- Oikos, Vol. 122, Issue 2
Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies
journal, August 2012
- Klindworth, Anna; Pruesse, Elmar; Schweer, Timmy
- Nucleic Acids Research, Vol. 41, Issue 1
Metabolic threshold and sulfide-buffering in diffusion controlled marine sediments impacted by continuous organic enrichment
journal, July 2009
- Valdemarsen, Thomas; Kristensen, Erik; Holmer, Marianne
- Biogeochemistry, Vol. 95, Issue 2-3
QIIME allows analysis of high-throughput community sequencing data
journal, April 2010
- Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
- Nature Methods, Vol. 7, Issue 5
On the Subdivision of the Phyllite-Nappe of Crete and Peloponnesus [Zur Gliederung der Phyllit-Decke Kretas und des Peloponnes]
journal, January 1994
- Dornsiepen, Ulrich Friedrich; Manutsoglu, Emmanuil
- Zeitschrift der Deutschen Geologischen Gesellschaft, Vol. 145, Issue 2
Flow Cytometric Assessment of Bacterial Abundance in Soils, Sediments and Sludge
journal, June 2016
- Frossard, Aline; Hammes, Frederik; Gessner, Mark O.
- Frontiers in Microbiology, Vol. 7
Extraction and purification of microbial DNA from soil and sediment samples
journal, September 2001
- Roose-Amsaleg, C. L.; Garnier-Sillam, E.; Harry, M.
- Applied Soil Ecology, Vol. 18, Issue 1
Niche specialization of terrestrial archaeal ammonia oxidizers
journal, December 2011
- Gubry-Rangin, C.; Hai, B.; Quince, C.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 52
Summary and overview of the CYCLOPS P addition Lagrangian experiment in the Eastern Mediterranean
journal, November 2005
- Krom, M. D.; Thingstad, T. F.; Brenner, S.
- Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 52, Issue 22-23
Testing for Phylogenetic Signal in Comparative Data: Behavioral Traits are more Labile
journal, April 2003
- Blomberg, Simon P.; Garland, Theodore; Ives, Anthony R.
- Evolution, Vol. 57, Issue 4
Picante: R tools for integrating phylogenies and ecology
journal, April 2010
- Kembel, S. W.; Cowan, P. D.; Helmus, M. R.
- Bioinformatics, Vol. 26, Issue 11
Microbial ecosystems are dominated by specialist taxa
journal, August 2015
- Mariadassou, Mahendra; Pichon, Samuel; Ebert, Dieter
- Ecology Letters, Vol. 18, Issue 9
Climate change and geothermal ecosystems: natural laboratories, sentinel systems, and future refugia
journal, June 2014
- O'Gorman, Eoin J.; Benstead, Jonathan P.; Cross, Wyatt F.
- Global Change Biology, Vol. 20, Issue 11
Spreading Dead Zones and Consequences for Marine Ecosystems
journal, August 2008
- Diaz, R. J.; Rosenberg, R.
- Science, Vol. 321, Issue 5891
The value of estuarine and coastal ecosystem services
journal, May 2011
- Barbier, Edward B.; Hacker, Sally D.; Kennedy, Chris
- Ecological Monographs, Vol. 81, Issue 2