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Title: Functional diversity and redundancy across fish gut, sediment and water bacterial communities

Abstract

Here, this work explores the functional diversity and redundancy in a bacterial metacommunity constituted of three habitats (sediment, water column and fish gut) in a coastal lagoon under anthropogenic pressure. Comprehensive functional gene arrays covering a wide range of ecological processes and stress resistance genes to estimate the functional potential of bacterial communities were used. Then, diversity partitioning was used to characterize functional diversity and redundancy within (α), between (β) and across (γ) habitats. It was showed that all local communities exhibit a highly diversified potential for the realization of key ecological processes and resistance to various environmental conditions, supporting the growing evidence that macro-organisms microbiomes harbour a high functional potential and are integral components of functional gene dynamics in aquatic bacterial metacommunities. Several levels of functional redundancy at different scales of the bacterial metacommunity were observed (within local communities, within habitats and at the metacommunity level). The findings indicated a high potential for the realization of spatial ecological insurance within this ecosystem, that is, the functional compensation among microorganisms for the realization and maintenance of key ecological processes, within and across habitats. Finally, the role of macro-organisms as dispersal vectors of microbes and their potential influence on marine metacommunitymore » dynamics were discussed.« less

Authors:
 [1];  [2];  [3];  [2];  [2];  [4];  [5];  [5];  [6];  [7]
  1. Univ. of Oklahoma, Norman, OK (United States)
  2. Université Montpellier (France). IRD‐CNRS‐UM‐IFREMER
  3. Institute for Environmental Genomics and Department of Microbiology and Plant BiologyUniversity of OklahomaNorman OK73019 USA
  4. National Museum of Natural History, Paris (France)
  5. Universidad Autonoma de Campeche (Mexico)
  6. Univ. of Oklahoma, Norman, OK (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Tsinghua Univ., Beijing (China)
  7. Université Montpellier (France). IRD‐CNRS‐UM‐IFREMER; James Cook Univ., Townsville, QLD (Australia)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1567090
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Volume: 19; Journal Issue: 8; Journal ID: ISSN 1462-2912
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Escalas, Arthur, Troussellier, Marc, Yuan, Tong, Bouvier, Thierry, Bouvier, Corinne, Mouchet, Maud A., Flores Hernandez, Domingo, Ramos Miranda, Julia, Zhou, Jizhong, and Mouillot, David. Functional diversity and redundancy across fish gut, sediment and water bacterial communities. United States: N. p., 2017. Web. doi:10.1111/1462-2920.13822.
Escalas, Arthur, Troussellier, Marc, Yuan, Tong, Bouvier, Thierry, Bouvier, Corinne, Mouchet, Maud A., Flores Hernandez, Domingo, Ramos Miranda, Julia, Zhou, Jizhong, & Mouillot, David. Functional diversity and redundancy across fish gut, sediment and water bacterial communities. United States. doi:10.1111/1462-2920.13822.
Escalas, Arthur, Troussellier, Marc, Yuan, Tong, Bouvier, Thierry, Bouvier, Corinne, Mouchet, Maud A., Flores Hernandez, Domingo, Ramos Miranda, Julia, Zhou, Jizhong, and Mouillot, David. Thu . "Functional diversity and redundancy across fish gut, sediment and water bacterial communities". United States. doi:10.1111/1462-2920.13822. https://www.osti.gov/servlets/purl/1567090.
@article{osti_1567090,
title = {Functional diversity and redundancy across fish gut, sediment and water bacterial communities},
author = {Escalas, Arthur and Troussellier, Marc and Yuan, Tong and Bouvier, Thierry and Bouvier, Corinne and Mouchet, Maud A. and Flores Hernandez, Domingo and Ramos Miranda, Julia and Zhou, Jizhong and Mouillot, David},
abstractNote = {Here, this work explores the functional diversity and redundancy in a bacterial metacommunity constituted of three habitats (sediment, water column and fish gut) in a coastal lagoon under anthropogenic pressure. Comprehensive functional gene arrays covering a wide range of ecological processes and stress resistance genes to estimate the functional potential of bacterial communities were used. Then, diversity partitioning was used to characterize functional diversity and redundancy within (α), between (β) and across (γ) habitats. It was showed that all local communities exhibit a highly diversified potential for the realization of key ecological processes and resistance to various environmental conditions, supporting the growing evidence that macro-organisms microbiomes harbour a high functional potential and are integral components of functional gene dynamics in aquatic bacterial metacommunities. Several levels of functional redundancy at different scales of the bacterial metacommunity were observed (within local communities, within habitats and at the metacommunity level). The findings indicated a high potential for the realization of spatial ecological insurance within this ecosystem, that is, the functional compensation among microorganisms for the realization and maintenance of key ecological processes, within and across habitats. Finally, the role of macro-organisms as dispersal vectors of microbes and their potential influence on marine metacommunity dynamics were discussed.},
doi = {10.1111/1462-2920.13822},
journal = {Environmental Microbiology},
number = 8,
volume = 19,
place = {United States},
year = {2017},
month = {6}
}

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Works referenced in this record:

Biodiversity and Resilience of Ecosystem Functions
journal, November 2015

  • Oliver, Tom H.; Heard, Matthew S.; Isaac, Nick J. B.
  • Trends in Ecology & Evolution, Vol. 30, Issue 11
  • DOI: 10.1016/j.tree.2015.08.009

Interactions in the microbiome: communities of organisms and communities of genes
journal, January 2014

  • Boon, Eva; Meehan, Conor J.; Whidden, Chris
  • FEMS Microbiology Reviews, Vol. 38, Issue 1
  • DOI: 10.1111/1574-6976.12035

Bacterial communities and species-specific associations with the mucus of Brazilian coral species
journal, April 2013

  • Carlos, Camila; Torres, Tatiana T.; Ottoboni, Laura M. M.
  • Scientific Reports, Vol. 3, Issue 1
  • DOI: 10.1038/srep01624

Chlorinated pesticides in the Rio Palizada, Campeche, Mexico
journal, November 1993


Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity
journal, July 2014


Biodiversity loss and its impact on humanity
journal, June 2012

  • Cardinale, Bradley J.; Duffy, J. Emmett; Gonzalez, Andrew
  • Nature, Vol. 486, Issue 7401
  • DOI: 10.1038/nature11148

Linking metacommunity theory and symbiont evolutionary ecology
journal, June 2012


Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance
journal, September 2007


Several scales of biodiversity affect ecosystem multifunctionality
journal, June 2013

  • Pasari, J. R.; Levi, T.; Zavaleta, E. S.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 25
  • DOI: 10.1073/pnas.1220333110

Fundamentals of Microbial Community Resistance and Resilience
journal, January 2012


Functional Redundancy-Induced Stability of Gut Microbiota Subjected to Disturbance
journal, May 2016


Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation
journal, September 2010

  • Villéger, Sébastien; Miranda, Julia Ramos; Hernández, Domingo Flores
  • Ecological Applications, Vol. 20, Issue 6
  • DOI: 10.1890/09-1310.1

Biodiversity enhances ecosystem reliability
journal, December 1997

  • Naeem, Shahid; Li, Shibin
  • Nature, Vol. 390, Issue 6659
  • DOI: 10.1038/37348

Animals in a bacterial world, a new imperative for the life sciences
journal, February 2013

  • McFall-Ngai, Margaret; Hadfield, Michael G.; Bosch, Thomas C. G.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 9
  • DOI: 10.1073/pnas.1218525110

Composition of Archaea in Seawater, Sediment, and Sponges in the Kepulauan Seribu Reef System, Indonesia
journal, January 2014

  • Polónia, Ana R. M.; Cleary, Daniel F. R.; Duarte, Leticia N.
  • Microbial Ecology, Vol. 67, Issue 3
  • DOI: 10.1007/s00248-013-0365-2

Biodiversity and ecosystem productivity in a fluctuating environment: The insurance hypothesis
journal, February 1999

  • Yachi, S.; Loreau, M.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 4
  • DOI: 10.1073/pnas.96.4.1463

Biodiversity and multifunctionality in a microbial community: a novel theoretical approach to quantify functional redundancy
journal, February 2014

  • Miki, Takeshi; Yokokawa, Taichi; Matsui, Kazuaki
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1776
  • DOI: 10.1098/rspb.2013.2498

Sustaining Rare Marine Microorganisms: Macroorganisms As Repositories and Dispersal Agents of Microbial Diversity
journal, May 2017


Experimental and analytical tools for studying the human microbiome
journal, December 2011

  • Kuczynski, Justin; Lauber, Christian L.; Walters, William A.
  • Nature Reviews Genetics, Vol. 13, Issue 1
  • DOI: 10.1038/nrg3129

Tides and currents in a two-inlet coastal lagoon: Laguna de Términos, México
journal, August 1998


Genetic difference but functional similarity among fish gut bacterial communities through molecular and biochemical fingerprints
journal, December 2011


Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota
journal, April 2015

  • Smith, Chris CR; Snowberg, Lisa K.; Gregory Caporaso, J.
  • The ISME Journal, Vol. 9, Issue 11
  • DOI: 10.1038/ismej.2015.64

Marine sponges as microbial fermenters: Marine sponges as microbial fermenters
journal, February 2006


Trace metals in the oyster Crasostrea virginica of the Terminos Lagoon, Campeche, Mexico
journal, July 1993


GeoChip-based analysis of the functional gene diversity and metabolic potential of soil microbial communities of mangroves
journal, November 2012

  • Bai, Shijie; Li, Jiangwei; He, Zhili
  • Applied Microbiology and Biotechnology, Vol. 97, Issue 15
  • DOI: 10.1007/s00253-012-4496-z

The Influence of Functional Diversity and Composition on Ecosystem Processes
journal, August 1997


Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs
journal, September 2014

  • Mouillot, D.; Villeger, S.; Parravicini, V.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 38
  • DOI: 10.1073/pnas.1317625111

Microbial functional structure of Montastraea faveolata , an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies
journal, February 2010


High plant diversity is needed to maintain ecosystem services
journal, August 2011

  • Isbell, Forest; Calcagno, Vincent; Hector, Andy
  • Nature, Vol. 477, Issue 7363
  • DOI: 10.1038/nature10282

Trait-based approaches for understanding microbial biodiversity and ecosystem functioning
journal, May 2014


Bacterial community assembly based on functional genes rather than species
journal, August 2011

  • Burke, C.; Steinberg, P.; Rusch, D.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 34
  • DOI: 10.1073/pnas.1101591108

Tropical Fishes as Biological Bulldozers: Density Effects on Resource Heterogeneity and Species Diversity
journal, August 2004

  • Flecker, Alexander S.; Taylor, Brad W.
  • Ecology, Vol. 85, Issue 8
  • DOI: 10.1890/03-0194

Loss of Rare Fish Species from Tropical Floodplain Food Webs Affects Community Structure and Ecosystem Multifunctionality in a Mesocosm Experiment
journal, January 2014


Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts
journal, June 2012

  • Fan, L.; Reynolds, D.; Liu, M.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 27
  • DOI: 10.1073/pnas.1203287109

Maintenance of soil functioning following erosion of microbial diversity
journal, December 2006


Function-specific response to depletion of microbial diversity
journal, August 2010

  • Peter, Hannes; Beier, Sara; Bertilsson, Stefan
  • The ISME Journal, Vol. 5, Issue 2
  • DOI: 10.1038/ismej.2010.119

Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity-function relationships
journal, November 2010


Composition and Predictive Functional Analysis of Bacterial Communities in Seawater, Sediment and Sponges in the Spermonde Archipelago, Indonesia
journal, June 2015

  • Cleary, Daniel F. R.; de Voogd, Nicole J.; Polónia, Ana R. M.
  • Microbial Ecology, Vol. 70, Issue 4
  • DOI: 10.1007/s00248-015-0632-5

Lack of functional redundancy in the relationship between microbial diversity and ecosystem functioning
journal, May 2016

  • Delgado-Baquerizo, Manuel; Giaramida, Luca; Reich, Peter B.
  • Journal of Ecology, Vol. 104, Issue 4
  • DOI: 10.1111/1365-2745.12585

More functional genes and convergent overall functional patterns detected by geochip in phenanthrene-spiked soils
journal, June 2012


Pesticide and PCB residues in the aquatic ecosystems of Laguna de Terminos, a protected area of the coast of Campeche, Mexico
journal, February 2009


Microarray-Based Analysis of Subnanogram Quantities of Microbial Community DNAs by Using Whole-Community Genome Amplification
journal, July 2006

  • Wu, L.; Liu, X.; Schadt, C. W.
  • Applied and Environmental Microbiology, Vol. 72, Issue 7
  • DOI: 10.1128/AEM.02738-05

Land use change alters functional gene diversity, composition and abundance in Amazon forest soil microbial communities
journal, June 2014

  • Paula, Fabiana S.; Rodrigues, Jorge L. M.; Zhou, Jizhong
  • Molecular Ecology, Vol. 23, Issue 12
  • DOI: 10.1111/mec.12786

Biodiversity and ecosystem services: a multilayered relationship
journal, January 2012

  • Mace, Georgina M.; Norris, Ken; Fitter, Alastair H.
  • Trends in Ecology & Evolution, Vol. 27, Issue 1
  • DOI: 10.1016/j.tree.2011.08.006

Biodiversity as spatial insurance in heterogeneous landscapes
journal, October 2003

  • Loreau, M.; Mouquet, N.; Gonzalez, A.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 22
  • DOI: 10.1073/pnas.2235465100

First insights into the microbiome of a carnivorous sponge
journal, August 2013

  • Dupont, Samuel; Corre, Erwan; Li, Yanyan
  • FEMS Microbiology Ecology, Vol. 86, Issue 3
  • DOI: 10.1111/1574-6941.12178

Depletion, Degradation, and Recovery Potential of Estuaries and Coastal Seas
journal, June 2006


Random Sampling Process Leads to Overestimation of β-Diversity of Microbial Communities
journal, June 2013


Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis
journal, November 2010

  • Burke, Catherine; Thomas, Torsten; Lewis, Matt
  • The ISME Journal, Vol. 5, Issue 4
  • DOI: 10.1038/ismej.2010.164

Strain/Species-Specific Probe Design for Microbial Identification Microarrays
journal, June 2013

  • Tu, Q.; He, Z.; Deng, Y.
  • Applied and Environmental Microbiology, Vol. 79, Issue 16
  • DOI: 10.1128/AEM.01124-13

GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes
journal, May 2007

  • He, Zhili; Gentry, Terry J.; Schadt, Christopher W.
  • The ISME Journal, Vol. 1, Issue 1
  • DOI: 10.1038/ismej.2007.2

High-Throughput Metagenomic Technologies for Complex Microbial Community Analysis: Open and Closed Formats
journal, January 2015


Temporal patterns of rarity provide a more complete view of microbial diversity
journal, June 2015


Bioinformatics for the Human Microbiome Project
journal, November 2012


The microbial gene diversity along an elevation gradient of the Tibetan grassland
journal, August 2013


Human-Mediated Loss of Phylogenetic and Functional Diversity in Coral Reef Fishes
journal, March 2014


General stabilizing effects of plant diversity on grassland productivity through population asynchrony and overyielding
journal, August 2010

  • Hector, A.; Hautier, Y.; Saner, P.
  • Ecology, Vol. 91, Issue 8
  • DOI: 10.1890/09-1162.1

Multifunctionality and Diversity in Bacterial Biofilms
journal, August 2011


Geo-Chip analysis reveals reduced functional diversity of the bacterial community at a dumping site for dredged Elbe sediment
journal, December 2013


Threatened Corals Provide Underexplored Microbial Habitats
journal, March 2010


Biodiversity, climate change, and ecosystem services
journal, October 2009

  • Mooney, Harold; Larigauderie, Anne; Cesario, Manuel
  • Current Opinion in Environmental Sustainability, Vol. 1, Issue 1
  • DOI: 10.1016/j.cosust.2009.07.006

Resilience of Amazon forests emerges from plant trait diversity
journal, August 2016

  • Sakschewski, Boris; von Bloh, Werner; Boit, Alice
  • Nature Climate Change, Vol. 6, Issue 11
  • DOI: 10.1038/nclimate3109

Ecosystem stability in space: α, β and γ variability
journal, May 2014

  • Wang, Shaopeng; Loreau, Michel
  • Ecology Letters, Vol. 17, Issue 8
  • DOI: 10.1111/ele.12292

Microbial mediation of biogeochemical cycles revealed by simulation of global changes with soil transplant and cropping
journal, April 2014


Changes in four complementary facets of fish diversity in a tropical coastal lagoon after 18 years: a functional interpretation
journal, January 2005

  • Ramos Miranda, J.; Mouillot, D.; Hernandez, Df
  • Marine Ecology Progress Series, Vol. 304
  • DOI: 10.3354/meps304001

GeoChip-based insights into the microbial functional gene repertoire of marine sponges (high microbial abundance, low microbial abundance) and seawater
journal, November 2014

  • Bayer, Kristina; Moitinho-Silva, Lucas; Brümmer, Franz
  • FEMS Microbiology Ecology, Vol. 90, Issue 3
  • DOI: 10.1111/1574-6941.12441

Microbial functional genes enriched in the Xiangjiang River sediments with heavy metal contamination
journal, August 2016


Phylogenetic conservatism of functional traits in microorganisms
journal, December 2012

  • Martiny, Adam C.; Treseder, Kathleen; Pusch, Gordon
  • The ISME Journal, Vol. 7, Issue 4
  • DOI: 10.1038/ismej.2012.160

Regional Variation in the Hierarchical Partitioning of Diversity in Coral-Dwelling Fishes
journal, October 2008

  • Belmaker, Jonathan; Ziv, Yaron; Shashar, Nadav
  • Ecology, Vol. 89, Issue 10
  • DOI: 10.1890/07-1464.1

Tidal migration and patterns in feeding of the four-eyed fish Anableps anableps L. in a north Brazilian mangrove
journal, February 2007


The metacommunity concept: a framework for multi-scale community ecology: The metacommunity concept
journal, June 2004


Dynamics of Microbial Community Composition and Function during In Situ Bioremediation of a Uranium-Contaminated Aquifer
journal, April 2011

  • Van Nostrand, Joy D.; Wu, Liyou; Wu, Wei-Min
  • Applied and Environmental Microbiology, Vol. 77, Issue 11
  • DOI: 10.1128/AEM.01981-10

Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development
journal, August 2015

  • Burns, Adam R.; Stephens, W. Zac; Stagaman, Keaton
  • The ISME Journal, Vol. 10, Issue 3
  • DOI: 10.1038/ismej.2015.142

Taxonomic and functional metagenomic profiling of gastrointestinal tract microbiome of the farmed adult turbot ( Scophthalmus maximus )
journal, July 2013

  • Xing, Mengxin; Hou, Zhanhui; Yuan, Jianbo
  • FEMS Microbiology Ecology, Vol. 86, Issue 3
  • DOI: 10.1111/1574-6941.12174

Functional metagenomic profiling of nine biomes
journal, March 2008

  • Dinsdale, Elizabeth A.; Edwards, Robert A.; Hall, Dana
  • Nature, Vol. 452, Issue 7187
  • DOI: 10.1038/nature06810

Ecological risk assessment of PCBs and other organic contaminant residues in Laguna de Terminos, Mexico
journal, January 2009

  • Carvalho, Fernando P.; Villeneuve, Jean-Pierre; Cattini, Chantal
  • Ecotoxicology, Vol. 18, Issue 4
  • DOI: 10.1007/s10646-008-0295-9

Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts
journal, September 2004

  • Hittinger, C. T.; Rokas, A.; Carroll, S. B.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 39
  • DOI: 10.1073/pnas.0404319101

Response diversity determines the resilience of ecosystems to environmental change: Response diversity and ecosystem resilience
journal, December 2012

  • Mori, Akira S.; Furukawa, Takuya; Sasaki, Takehiro
  • Biological Reviews, Vol. 88, Issue 2
  • DOI: 10.1111/brv.12004

Biodiversity, productivity, and the spatial insurance hypothesis revisited
journal, September 2015


Functional gene diversity of soil microbial communities from five oil-contaminated fields in China
journal, September 2010


Resuscitation of the rare biosphere contributes to pulses of ecosystem activity
journal, January 2015


Biodiversity enhances ecosystem multifunctionality across trophic levels and habitats
journal, April 2015

  • Lefcheck, Jonathan S.; Byrnes, Jarrett E. K.; Isbell, Forest
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms7936

Biodiversity increases the resistance of ecosystem productivity to climate extremes
journal, October 2015

  • Isbell, Forest; Craven, Dylan; Connolly, John
  • Nature, Vol. 526, Issue 7574
  • DOI: 10.1038/nature15374

Linkages between biodiversity attributes and ecosystem services: A systematic review
journal, September 2014


Diet Drives Convergence in Gut Microbiome Functions Across Mammalian Phylogeny and Within Humans
journal, May 2011


Bacterial diversity promotes community stability and functional resilience after perturbation
journal, March 2005


Warming Alters Expressions of Microbial Functional Genes Important to Ecosystem Functioning
journal, May 2016


Polynuclear Aromatic Hydrocarbons in American Oysters Crassostrea virginica from the Terminos Lagoon, Campeche, Mexico
journal, August 1999

  • Noreña-Barroso, Elsa; Gold-Bouchot, Gerardo; zapata-perez, Omar
  • Marine Pollution Bulletin, Vol. 38, Issue 8
  • DOI: 10.1016/S0025-326X(98)00165-9

Comparative Analysis of the Intestinal Bacterial Communities in Different Species of Carp by Pyrosequencing
journal, August 2014


Spatial and Temporal Hydrological Variations in the Inner Estuaries of a Large Coastal Lagoon of the Southern Gulf of Mexico
journal, November 2015

  • Medina-Gómez, Israel; Villalobos-Zapata, Guillermo J.; Herrera-Silveira, Jorge A.
  • Journal of Coastal Research, Vol. 316
  • DOI: 10.2112/JCOASTRES-D-13-00226.1

Multiple Functions Increase the Importance of Biodiversity for Overall Ecosystem Functioning
journal, May 2008

  • Gamfeldt, Lars; Hillebrand, Helmut; Jonsson, Per R.
  • Ecology, Vol. 89, Issue 5
  • DOI: 10.1890/06-2091.1