Evolution of a Vegetarian Vibrio: Metabolic Specialization of Vibrio breoganii to Macroalgal Substrates
Abstract
While most Vibrionaceae are considered generalists that thrive on diverse substrates, including animal-derived material, we show that Vibrio breoganii has specialized for the consumption of marine macroalga-derived substrates. Genomic and physiological comparisons of V. breoganii with other Vibrionaceae isolates revealed the ability to degrade alginate, laminarin, and additional glycans present in algal cell walls. Moreover, the widely conserved ability to hydrolyze animal-derived polymers, including chitin and glycogen, was lost, along with the ability to efficiently grow on a variety of amino acids. Ecological data showing associations with particulate algal material but not zooplankton further support this shift in niche preference, and the loss of motility appears to reflect a sessile macroalga-associated lifestyle. Altogether, these findings indicate that algal polysaccharides have become a major source of carbon and energy in V. breoganii, and these ecophysiological adaptations may facilitate transient commensal associations with marine invertebrates that feed on algae.
- Authors:
-
[1];
- Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
- Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Univ. of Bremen Max Planck Inst. for Marine Microbiology, Bremen (Germany)
- Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Khalifa Univ. of Science and Technology, Abu Dhabi (United Arab of Emirates)
- Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Johns Hopkins Univ., Baltimore, MD (United States)
- Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Broad Inst., Cambridge, MA (United States)
- Michigan State Univ., East Lansing, MI (United States)
- Publication Date:
- Research Org.:
- Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1541705
- Grant/Contract Number:
- SC0008743
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Bacteriology
- Additional Journal Information:
- Journal Volume: 200; Journal Issue: 15; Journal ID: ISSN 0021-9193
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; microbiology; macroalgal carbohydrates; horizontal gene transfer; metabolic specialization; Vibrionaceae; ecology; adaptation; macroalgae; seaweed; Vibrio; algae; degradation; polysaccharide
Citation Formats
Corzett, Christopher H., Elsherbini, Joseph, Chien, Diana M., Hehemann, Jan-Hendrik, Henschel, Andreas, Preheim, Sarah P., Yu, Xiaoqian, Alm, Eric J., Polz, Martin F., and DiRita, Victor J. Evolution of a Vegetarian Vibrio: Metabolic Specialization of Vibrio breoganii to Macroalgal Substrates. United States: N. p., 2018.
Web. doi:10.1128/jb.00020-18.
Corzett, Christopher H., Elsherbini, Joseph, Chien, Diana M., Hehemann, Jan-Hendrik, Henschel, Andreas, Preheim, Sarah P., Yu, Xiaoqian, Alm, Eric J., Polz, Martin F., & DiRita, Victor J. Evolution of a Vegetarian Vibrio: Metabolic Specialization of Vibrio breoganii to Macroalgal Substrates. United States. https://doi.org/10.1128/jb.00020-18
Corzett, Christopher H., Elsherbini, Joseph, Chien, Diana M., Hehemann, Jan-Hendrik, Henschel, Andreas, Preheim, Sarah P., Yu, Xiaoqian, Alm, Eric J., Polz, Martin F., and DiRita, Victor J. Mon .
"Evolution of a Vegetarian Vibrio: Metabolic Specialization of Vibrio breoganii to Macroalgal Substrates". United States. https://doi.org/10.1128/jb.00020-18. https://www.osti.gov/servlets/purl/1541705.
@article{osti_1541705,
title = {Evolution of a Vegetarian Vibrio: Metabolic Specialization of Vibrio breoganii to Macroalgal Substrates},
author = {Corzett, Christopher H. and Elsherbini, Joseph and Chien, Diana M. and Hehemann, Jan-Hendrik and Henschel, Andreas and Preheim, Sarah P. and Yu, Xiaoqian and Alm, Eric J. and Polz, Martin F. and DiRita, Victor J.},
abstractNote = {While most Vibrionaceae are considered generalists that thrive on diverse substrates, including animal-derived material, we show that Vibrio breoganii has specialized for the consumption of marine macroalga-derived substrates. Genomic and physiological comparisons of V. breoganii with other Vibrionaceae isolates revealed the ability to degrade alginate, laminarin, and additional glycans present in algal cell walls. Moreover, the widely conserved ability to hydrolyze animal-derived polymers, including chitin and glycogen, was lost, along with the ability to efficiently grow on a variety of amino acids. Ecological data showing associations with particulate algal material but not zooplankton further support this shift in niche preference, and the loss of motility appears to reflect a sessile macroalga-associated lifestyle. Altogether, these findings indicate that algal polysaccharides have become a major source of carbon and energy in V. breoganii, and these ecophysiological adaptations may facilitate transient commensal associations with marine invertebrates that feed on algae.},
doi = {10.1128/jb.00020-18},
journal = {Journal of Bacteriology},
number = 15,
volume = 200,
place = {United States},
year = {Mon Apr 09 00:00:00 EDT 2018},
month = {Mon Apr 09 00:00:00 EDT 2018}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 12 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Acetic acid production of Vibrio halioticoli from alginate: a possible role for establishment of abalone–V. halioticoli association
journal, April 2003
- Sawabe, Tomoo; Setoguchi, Naka; Inoue, Sahoko
- Aquaculture, Vol. 219, Issue 1-4
Chitin and products of its hydrolysis in Vibrio cholerae ecology
journal, September 2015
- Markov, E. Yu.; Kulikalova, E. S.; Urbanovich, L. Ya.
- Biochemistry (Moscow), Vol. 80, Issue 9
Reproducibility of Vibrionaceae population structure in coastal bacterioplankton
journal, November 2012
- Szabo, Gitta; Preheim, Sarah P.; Kauffman, Kathryn M.
- The ISME Journal, Vol. 7, Issue 3
Population Genomics of Early Events in the Ecological Differentiation of Bacteria
journal, April 2012
- Shapiro, B. Jesse; Friedman, Jonathan; Cordero, Otto X.
- Science, Vol. 336, Issue 6077
Analysis of bacterial community and bacterial nutritional enzyme activity associated with the digestive tract of wild Chilean octopus ( Octopus mimus Gould, 1852)
journal, July 2013
- Iehata, Shunpei; Valenzuela, Fernando; Riquelme, Carlos
- Aquaculture Research, Vol. 46, Issue 4
Metapopulation structure of Vibrionaceae among coastal marine invertebrates
journal, September 2010
- Preheim, Sarah P.; Boucher, Yan; Wildschutte, Hans
- Environmental Microbiology, Vol. 13, Issue 1
Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations
journal, April 2014
- Yawata, Y.; Cordero, O. X.; Menolascina, F.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 15
Interactions of Vibrio spp. with Zooplankton
journal, June 2015
- Erken, Martina; Lutz, Carla; McDougald, Diane
- Microbiology Spectrum, Vol. 3, Issue 3
Trade-off Mechanisms Shaping the Diversity of Bacteria
journal, March 2016
- Ferenci, Thomas
- Trends in Microbiology, Vol. 24, Issue 3
Associations and dynamics of Vibrionaceae in the environment, from the genus to the population level
journal, January 2014
- Takemura, Alison F.; Chien, Diana M.; Polz, Martin F.
- Frontiers in Microbiology, Vol. 5
An Engineered Microbial Platform for Direct Biofuel Production from Brown Macroalgae
journal, January 2012
- Wargacki, A. J.; Leonard, E.; Win, M. N.
- Science, Vol. 335, Issue 6066
Stable Associations Masked by Temporal Variability in the Marine Copepod Microbiome
journal, September 2015
- Moisander, Pia H.; Sexton, Andrew D.; Daley, Meaghan C.
- PLOS ONE, Vol. 10, Issue 9
Molecular Analysis of Bacterial Microbiota Associated with Oysters (Crassostrea gigas and Crassostrea corteziensis) in Different Growth Phases at Two Cultivation Sites
journal, March 2012
- Trabal, Natalia; Mazón-Suástegui, José M.; Vázquez-Juárez, Ricardo
- Microbial Ecology, Vol. 64, Issue 2
A genomic comparison of 13 symbiotic Vibrio fischeri isolates from the perspective of their host source and colonization behavior
journal, April 2016
- Bongrand, Clotilde; Koch, Eric J.; Moriano-Gutierrez, Silvia
- The ISME Journal, Vol. 10, Issue 12
Natural resource landscapes of a marine bacterium reveal distinct fitness-determining genes across the genome: Natural resource landscapes of a marine bacterium
journal, May 2017
- Takemura, Alison F.; Corzett, Christopher H.; Hussain, Fatima
- Environmental Microbiology, Vol. 19, Issue 6
Global impact of Vibrio cholerae interactions with chitin: V. cholerae - chitin interactions
journal, February 2008
- Pruzzo, Carla; Vezzulli, Luigi; Colwell, Rita R.
- Environmental Microbiology, Vol. 10, Issue 6
In-depth metabolic profiling of marine macroalgae confirms strong biochemical differences between brown, red and green algae
journal, September 2017
- Belghit, Ikram; Rasinger, Josef D.; Heesch, Svenja
- Algal Research, Vol. 26
Characterization of Potential Polysaccharide Utilization Systems in the Marine Bacteroidetes Gramella Flava JLT2011 Using a Multi-Omics Approach
journal, February 2017
- Tang, Kai; Lin, Yingfan; Han, Yu
- Frontiers in Microbiology, Vol. 8
Colloidal chitin stained with Remazol Brilliant Blue R®, a useful substrate to select chitinolytic microorganisms and to evaluate chitinases
journal, February 2004
- Gómez Ramı́rez, M.; Rojas Avelizapa, L. I.; Rojas Avelizapa, N. G.
- Journal of Microbiological Methods, Vol. 56, Issue 2
Adaptive radiation by waves of gene transfer leads to fine-scale resource partitioning in marine microbes
journal, September 2016
- Hehemann, Jan-Hendrik; Arevalo, Philip; Datta, Manoshi S.
- Nature Communications, Vol. 7, Issue 1
Persistence of vibrios in marine bivalves: the role of interactions with haemolymph components: Vibrio interactions with marine bivalve haemolymph
journal, April 2005
- Pruzzo, Carla; Gallo, Gabriella; Canesi, Laura
- Environmental Microbiology, Vol. 7, Issue 6
dbCAN: a web resource for automated carbohydrate-active enzyme annotation
journal, May 2012
- Yin, Yanbin; Mao, Xizeng; Yang, Jincai
- Nucleic Acids Research, Vol. 40, Issue W1
The Genome of the Alga-Associated Marine Flavobacterium Formosa agariphila KMM 3901 T Reveals a Broad Potential for Degradation of Algal Polysaccharides
journal, August 2013
- Mann, Alexander J.; Hahnke, Richard L.; Huang, Sixing
- Applied and Environmental Microbiology, Vol. 79, Issue 21
Extraction, structure and biofunctional activities of laminarin from brown algae
journal, December 2014
- Kadam, Shekhar U.; Tiwari, Brijesh K.; O'Donnell, Colm P.
- International Journal of Food Science & Technology, Vol. 50, Issue 1
Distribution of Vibrio halioticoli around an Abalone-farming Center in Japan
journal, January 2002
- Tanaka, Reiji; Sawabe, Tomoo; Yoshimizu, Mamoru
- Microbes and Environments, Vol. 17, Issue 1
Biodiversity of Vibrios
journal, September 2004
- Thompson, F. L.; Iida, T.; Swings, J.
- Microbiology and Molecular Biology Reviews, Vol. 68, Issue 3
Exploiting fine-scale genetic and physiological variation of closely related microbes to reveal unknown enzyme functions
journal, June 2017
- Badur, Ahmet H.; Plutz, Matthew J.; Yalamanchili, Geethika
- Journal of Biological Chemistry, Vol. 292, Issue 31
Microbial interactions lead to rapid micro-scale successions on model marine particles
journal, June 2016
- Datta, Manoshi S.; Sliwerska, Elzbieta; Gore, Jeff
- Nature Communications, Vol. 7, Issue 1
Diversity and Dynamics of a North Atlantic Coastal Vibrio Community
journal, July 2004
- Thompson, J. R.; Randa, M. A.; Marcelino, L. A.
- Applied and Environmental Microbiology, Vol. 70, Issue 7
The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013
- Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
- Nucleic Acids Research, Vol. 42, Issue D1
Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes
journal, October 2006
- Polz, Martin F.; Hunt, Dana E.; Preheim, Sarah P.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 361, Issue 1475
Enzymatic deconstruction of xylan for biofuel production
journal, February 2009
- Dodd, Dylan; Cann, Isaac K. O.
- GCB Bioenergy, Vol. 1, Issue 1
Glycogen and its metabolism: some new developments and old themes
journal, January 2012
- Roach, Peter J.; Depaoli-Roach, Anna A.; Hurley, Thomas D.
- Biochemical Journal, Vol. 441, Issue 3
Characterization of polysaccharides extracted from brown seaweeds
journal, June 2007
- Rioux, L. -E.; Turgeon, S. L.; Beaulieu, M.
- Carbohydrate Polymers, Vol. 69, Issue 3
Looking for Darwin's footprints in the microbial world
journal, May 2009
- Shapiro, B. Jesse; David, Lawrence A.; Friedman, Jonathan
- Trends in Microbiology, Vol. 17, Issue 5
Vibrio breoganii sp. nov., a non-motile, alginolytic, marine bacterium within the Vibrio halioticoli clade
journal, June 2009
- Beaz Hidalgo, R.; Cleenwerck, I.; Balboa, S.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 7
Metabolic competition as a driver of bacterial population structure
journal, October 2016
- Watkins, Eleanor R.; Maiden, Martin CJ; Gupta, Sunetra
- Future Microbiology, Vol. 11, Issue 10
New Vibrio species associated to molluscan microbiota: a review
journal, January 2014
- Romalde, Jesús L.; Dieguez, Ana L.; Lasa, Aide
- Frontiers in Microbiology, Vol. 4
The Evolution of Ecological Specialization
journal, November 1988
- Futuyma, D. J.; Moreno, G.
- Annual Review of Ecology and Systematics, Vol. 19, Issue 1
Sympatric Speciation: When Is It Possible in Bacteria?
journal, January 2013
- Friedman, Jonathan; Alm, Eric J.; Shapiro, B. Jesse
- PLoS ONE, Vol. 8, Issue 1
Functional characterization of polysaccharide utilization loci in the marine Bacteroidetes ‘Gramella forsetii’ KT0803
journal, February 2014
- Kabisch, Antje; Otto, Andreas; König, Sten
- The ISME Journal, Vol. 8, Issue 7
Laminarin favorably modulates gut microbiota in mice fed a high-fat diet
journal, January 2016
- Nguyen, Son G.; Kim, Jungman; Guevarra, Robin B.
- Food & Function, Vol. 7, Issue 10
Merging Taxonomy with Ecological Population Prediction in a Case Study of Vibrionaceae
journal, August 2011
- Preheim, Sarah P.; Timberlake, Sonia; Polz, Martin F.
- Applied and Environmental Microbiology, Vol. 77, Issue 20
The presence, nature, and role of gut microflora in aquatic invertebrates: A synthesis
journal, May 1993
- Harris, JeanM.
- Microbial Ecology, Vol. 25, Issue 3
Persistence, Seasonal Dynamics and Pathogenic Potential of Vibrio Communities from Pacific Oyster Hemolymph
journal, April 2014
- Wendling, Carolin C.; Batista, Frederico M.; Wegner, K. Mathias
- PLoS ONE, Vol. 9, Issue 4
Characterization of nitrogen-fixing bacteria from a temperate saltmarsh lagoon, including isolates that produce ethane from acetylene
journal, January 1994
- Tibbles, B. J.; Rawlings, D. E.
- Microbial Ecology, Vol. 27, Issue 1
Structure and function of α-glucan debranching enzymes
journal, May 2016
- Møller, Marie Sofie; Henriksen, Anette; Svensson, Birte
- Cellular and Molecular Life Sciences, Vol. 73, Issue 14
Vibrio halioticoli sp. nov., a non-motile alginolytic marine bacterium isolated from the gut of the abalone Haliotis discus hannai
journal, April 1998
- Sawabe, T.; Sugimura, I.; Ohtsuka, M.
- International Journal of Systematic Bacteriology, Vol. 48, Issue 2
Alginate degradation by bacteria isolated from the gut of sea urchins and abalones
journal, September 1995
- Sawabe, T.; Oda, Y.; Shiomi, Y.
- Microbial Ecology, Vol. 30, Issue 2
Conservation of the Chitin Utilization Pathway in the Vibrionaceae
journal, October 2007
- Hunt, D. E.; Gevers, D.; Vahora, N. M.
- Applied and Environmental Microbiology, Vol. 74, Issue 1
Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes
journal, January 2013
- Levasseur, Anthony; Drula, Elodie; Lombard, Vincent
- Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41
Molecular profiling of microbial community structure and their CAZymes via metagenomics, from Tsomgo lake in the Eastern Himalayas
journal, April 2021
- Rai, Aditi; Bhattacharjee, Arindam
- Archives of Microbiology, Vol. 203, Issue 6
Microbial interactions lead to rapid micro-scale successions on model marine particles
text, January 2016
- Datta, Manoshi S.; Sliwerska, Elzbieta; Gore, Jeff
- ETH Zurich
Works referencing / citing this record:
Host-associated microbiomes drive structure and function of marine ecosystems
journal, November 2019
- Wilkins, Laetitia G. E.; Leray, Matthieu; O’Dea, Aaron
- PLOS Biology, Vol. 17, Issue 11
Host-associated microbiomes drive structure and function of marine ecosystems
journal, November 2019
- Wilkins, Laetitia G. E.; Leray, Matthieu; O’Dea, Aaron
- PLOS Biology, Vol. 17, Issue 11