skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Metatranscriptomics and Amplicon Sequencing Reveal Mutualisms in Seagrass Microbiomes

Journal Article · · Frontiers in Microbiology
 [1];  [1];  [2];  [3]
  1. Oregon State Univ., Corvallis, OR (United States). College of Earth, Ocean and Atmospheric Sciences
  2. Oregon State Univ., Corvallis, OR (United States). Dept. of Fisheries and Wildlife; Universitat de les Illes Balears (UIB), Esporles (Spain). Instituto Mediterraneo de Estudios Avanzados (IMEDEA). Consejo Superior de Investigaciones Cientificas (CSIC)
  3. Oregon State Univ., Corvallis, OR (United States). Dept. of Mircobiology

Terrestrial plants benefit from many well-understood mutualistic relationships with root and leaf-associated microbiomes, but relatively little is known about these relationships for seagrass and other aquatic plants. We used 16S rRNA gene amplicon sequencing and metatranscriptomics to assess potential mutualisms between microorganisms and the seagrasses Zostera marina and Zostera japonica collected from mixed beds in Netarts Bay, OR, United States. The phylogenetic composition of leaf-, root-, and water column-associated bacterial communities were strikingly different, but these communities were not significantly different between plant species. Many taxa present on leaves were related to organisms capable of consuming the common plant metabolic waste product methanol, and of producing agarases, which can limit the growth of epiphytic algae. Taxa present on roots were related to organisms capable of oxidizing toxic sulfur compounds and of fixing nitrogen. Metatranscriptomic sequencing identified expression of genes involved in all of these microbial metabolic processes at levels greater than typical water column bacterioplankton, and also identified expression of genes involved in denitrification and in bacterial synthesis of the plant growth hormone indole-3-acetate. These results provide the first evidence using metatranscriptomics that seagrass microbiomes carry out a broad range of functions that may benefit their hosts, and imply that microbe–plant mutualisms support the health and growth of aquatic plants.

Research Organization:
Oregon State Univ., Corvallis, OR (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1628164
Journal Information:
Frontiers in Microbiology, Vol. 9; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English

References (118)

Photosynthetic responses of eelgrass (Zostera marina L.) to light and sediment sulfide in a shallow barrier island lagoon journal April 1995
Prokaryotic sulfur oxidation journal June 2005
Sulfide Intrusion and Detoxification in the Seagrass Zostera marina journal June 2015
Competitive Interactions in Mixed-Species Biofilms Containing the Marine Bacterium Pseudoalteromonas tunicata journal April 2005
Ecosystem services returned through seagrass restoration: Restoration of ecosystem services journal April 2016
Granulosicoccus coccoides sp. nov., isolated from leaves of seagrass (Zostera marina) journal April 2010
Overview of the physiological ecology of carbon metabolism in seagrasses journal July 2000
Marine epibiosis. I. Fouling and antifouling: some basic aspects journal January 1989
A native plant growth promoting bacterium, Bacillus sp. B55, rescues growth performance of an ethylene-insensitive plant genotype in nature journal January 2012
Biosynthesis of Organic Compounds Emitted by Plants journal March 1999
Simiduia curdlanivorans sp. nov., a curdlan-degrading bacterium isolated from the junction between the ocean and a freshwater spring, and emended description of the genus Simiduia journal November 2014
Spatial and temporal patterns in abundance of two intertidal seagrasses, Zostera americana den hartog and Zostera marina L. journal January 1982
Vanishing Seagrass (Zostera marina, L.) in Swedish Coastal Waters journal August 2003
Factors influencing the growth of seagrass seedlings: A case study of Posidonia australis journal January 2015
Habitat-specific distinctions in estuarine denitrification affect both ecosystem function and services journal January 2011
Methanol Emission from Leaves (Enzymatic Detection of Gas-Phase Methanol and Relation of Methanol Fluxes to Stomatal Conductance and Leaf Development) journal August 1995
Methanol:coenzyme M methyltransferase from Methanosarcina barkeri  -- substitution of the corrinoid harbouring subunit MtaC by free cob(I)alamin : Substitution of journal May 1999
Epiphytic bacterial communities on two common submerged macrophytes in Taihu Lake: diversity and host-specificity journal March 2012
Bacterial biosynthesis of indole-3-acetic acid journal March 1996
Complete genome sequence of Arcobacter nitrofigilis type strain (CIT) journal June 2010
Denitrification, nitrogen fixation, community primary productivity and inorganic-N and oxygen fluxes in an intertidal Zostera noltii meadow journal January 2000
Rhizosphere Microbiomes of European + Seagrasses Are Selected by the Plant, But Are Not Species Specific journal March 2016
The balance between nitrogen fixation and denitrification on vegetated and non-vegetated intertidal sediments: Nitrogen cycling in intertidal seagrass meadows journal July 2016
Supporting community annotation and user collaboration in the integrated microbial genomes (IMG) system journal April 2016
Novel mycoviruses discovered from metatranscriptomics survey of soybean phyllosphere phytobiomes journal February 2016
Effects of epibiotic bacteria on leaf growth and epiphytes of the seagrass Posidonia oceanica journal June 2012
The enhancement of plant growth by free-living bacteria journal February 1995
The rhizosphere microbiome and plant health journal August 2012
Molecular diversity of diazotrophs in oligotrophic tropical seagrass bed communities journal February 2002
Ethanol-Induced Injuries to Carrot Cells: The Role of Acetaldehyde journal March 1991
Denitrification, N-fixation and nitrogen and phosphorus fluxes in different benthic habitats and their contribution to the nitrogen and phosphorus budgets of a shallow oligotrophic sub-tropical coastal system (southern Moreton Bay, Australia) journal March 2010
Sedimenticola thiotaurini sp. nov., a sulfur-oxidizing bacterium isolated from salt marsh sediments, and emended descriptions of the genus Sedimenticola and Sedimenticola selenatireducens journal August 2015
Indole-3-acetic acid production by pink-pigmented facultative methylotrophic bacteria journal May 2004
MONOAMINE OXIDASE: From Genes to Behavior journal March 1999
A novel hydrogen oxidizer amidst the sulfur-oxidizing Thiomicrospira lineage journal September 2014
Sulphide intrusion in eelgrass (Zostera marina L.) journal May 2004
A Model For the Lowering of Plant Ethylene Concentrations by Plant Growth-promoting Bacteria journal January 1998
Integrative analysis of environmental sequences using MEGAN4 journal June 2011
Phylogenetic Analysis of Bacterial Communities Associated with Leaves of the Seagrass Halophila stipulacea by a Culture-Independent Small-Subunit rRNA Gene Approach journal January 2000
Science and Management of the Introduced Seagrass Zostera japonica in North America journal October 2013
Generation and possible roles of NO in plant roots and their apoplastic space journal December 2002
Algicidal and growth-inhibiting bacteria associated with seagrass and macroalgae beds in Puget Sound, WA, USA journal February 2017
Eutrophication in shallow coastal bays and lagoons: the role of plants in the coastal filter journal October 2007
A Global Crisis for Seagrass Ecosystems journal January 2006
An Earth-system perspective of the global nitrogen cycle journal January 2008
Nitrogen fixation in the rhizosphere of marine angiosperms journal September 1972
Cloning and Characterization of a Novel Agarase from a Newly Isolated Bacterium Simiduia sp. Strain TM-2 Able to Degrade Various Seaweeds journal July 2015
Metatranscriptome analysis reveals host-microbiome interactions in traps of carnivorous Genlisea species journal July 2015
Differences in Bacterial Community Structure on Hydrilla verticillata and Vallisneria americana in a Freshwater Spring journal January 2014
Two Potential Indole-3-Acetaldehyde Dehydrogenases in the Phytopathogenic Fungus Ustilago maydis journal December 1996
Illumina-based analysis the microbial diversity associated with Thalassia hemprichii in Xincun Bay, South China Sea journal June 2015
Ethylene production and decomposition in soils journal April 1998
A Three-Stage Symbiosis Forms the Foundation of Seagrass Ecosystems journal June 2012
Investigation of the role of a β(1–4) agarase produced by Pseudoalteromonas gracilis B9 in eliciting disease symptoms in the red alga Gracilaria gracilis journal October 2003
Coastal Ecosystems: A Critical Element of Risk Reduction: Coastal ecosystems and risk reduction journal November 2013
Microbial interactions and biocontrol in the rhizosphere journal March 2001
Relationship between productivity and N 2 (C 2 H 2 ) fixation in a Thalassia testudinum community1: Productivity and N 2 fixation journal January 1979
Distinct pattern of zeatin distribution in the shoot apical meristem marks stress conditions in Posidonia oceanica (L.) Delile plants journal March 2009
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms journal March 2012
Different niches of the Halophila stipulacea seagrass bed harbor distinct populations of nitrogen fixing bacteria journal June 1994
Diversity of uncultured microorganisms associated with the seagrass Halophila stipulacea estimated by restriction fragment length polymorphism analysis of PCR-amplified 16S rRNA genes. journal January 1996
Expansion of seagrass habitat by the exotic Zostera lapontca. and its use by dabbling ducks and brant in Boundary Bay, British Columbia journal January 1994
UPARSE: highly accurate OTU sequences from microbial amplicon reads journal August 2013
Temperate Wetland Methanogenesis: The Importance of Vegetation Type and Root Ethanol Production journal January 2010
Molecular cloning in Escherichia coli, expression, and nucleotide sequence of the gene for the ethylene-forming enzyme of Pseudomonas syringae pv. phaseolicola PK2 journal October 1992
Impact of light limitation on seagrasses journal November 2007
Role of Methylotrophy During Symbiosis Between Methylobacterium nodulans and Crotalaria podocarpa journal October 2005
The globally widespread genus Sulfurimonas: versatile energy metabolisms and adaptations to redox clines journal September 2015
Different bacterial communities associated with the roots and bulk sediment of the seagrass Zostera marina: Zostera marina: root-associated bacteria journal October 2007
Effects of anaerobiosis on root metabolism of Zostera marina (eelgrass): implications for survival in reducing sediments journal May 1988
In vitro culture of the seagrass Halophila decipiens journal April 1998
Seagrass landscapes and their effects on associated fauna: A review journal July 2006
Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria journal May 2015
CHARACTERIZATION AND COMPARISON OF PROKARYOTIC EPIPHYTES ASSOCIATED WITH THREE EAST AFRICAN SEAGRASSES 1 journal August 2007
The plant microbiome journal June 2013
The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea journal January 2016
C YTOKININ M ETABOLISM AND A CTION journal June 2001
Ribo-Zero Gold Kit: improved RNA-seq results after removal of cytoplasmic and mitochondrial ribosomal RNA journal October 2011
High rates of microbial dinitrogen fixation and sulfate reduction associated with the Mediterranean seagrass Posidonia oceanica journal October 2016
Assessing the ecological status of seagrasses using morphology, biochemical descriptors and microbial community analyses. A study in Halophila stipulacea (Forsk.) Aschers meadows in the northern Red Sea journal January 2016
Horizontal Gene Transfer from Diverse Bacteria to an Insect Genome Enables a Tripartite Nested Mealybug Symbiosis journal June 2013
The human gene for diamine oxidase, an amiloride binding protein. Molecular cloning, sequencing, and characterization of the promoter. journal May 1994
Soil beneficial bacteria and their role in plant growth promotion: a review journal August 2010
Reconciling the incompatible: N2 fixation And O2 journal December 1992
Analyzing Gene Expression from Marine Microbial Communities using Environmental Transcriptomics journal January 2009
Microbial Gene Abundance and Expression Patterns across a River to Ocean Salinity Gradient journal November 2015
Promotion of Plant Growth by Bacterial ACC Deaminase journal October 2007
Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples journal August 2012
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph journal January 2015
The effect of flooding on the exchange of the volatile C2-compounds ethanol, acetaldehyde and acetic acid between leaves of Amazonian floodplain tree species and the atmosphere journal January 2008
Nitrogen cycling in two temperate Zostera marina beds:seasonal variation journal January 2000
Rhizobacterial mediation of plant hormone status journal October 2010
Identity of major sulfur-cycle prokaryotes in freshwater lake ecosystems revealed by a comprehensive phylogenetic study of the dissimilatory adenylylsulfate reductase journal November 2016
Overexpression of bacterial ethylene-forming enzyme gene in Trichoderma reesei enhanced the production of ethylene journal January 2010
AtIPT3 is a Key Determinant of Nitrate-Dependent Cytokinin Biosynthesis in Arabidopsis journal August 2004
Microbial communities in sediment from Zostera marina patches, but not the Z. marina leaf or root microbiomes, vary in relation to distance from patch edge journal January 2017
Molecular interaction between Methylobacterium extorquens and seedlings: growth promotion, methanol consumption, and localization of the methanol emission site journal November 2006
Effects of some plant growth regulators on the growth of the seagrass Cymodocea nodosa (Ucria) Ascherson journal August 1995
Development and quantitative analyses of a universal rRNA-subtraction protocol for microbial metatranscriptomics journal March 2010
Attached Bacterial Populations Shared by Four Species of Aquatic Angiosperms journal August 2008
QIIME allows analysis of high-throughput community sequencing data journal April 2010
Bacterioplankton Community Shifts in an Arctic Lake Correlate with Seasonal Changes in Organic Matter Source journal April 2003
Genome-wide survey of the seagrass Zostera muelleri suggests modification of the ethylene signalling network journal January 2015
Plant host habitat and root exudates shape soil bacterial community structure journal August 2008
Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria journal August 1980
Nitrogen fixation associated with four species of submerged angiosperms in the central Chesapeake bay journal December 1979
Distribution and Evolution of Nitrogen Fixation Genes in the Phylum Bacteroidetes journal January 2015
Infant gut microbiota characteristics generally do not modify effects of lipid-based nutrient supplementation on growth or inflammation: secondary analysis of a randomized controlled trial in Malawi journal September 2020
Microbial Communities and Their Interactions in Soil and Rhizosphere Ecosystems journal October 2002
Microbial life in the phyllosphere journal November 2012
T-DNA of Agrobacterium tumefaciens encodes an enzyme of cytokinin biosynthesis. journal October 1984
Nitrogen Fixation by Epiphytes on sea Grasses1 journal March 1972
Indole-3-acetic acid in microbial and microorganism-plant signaling journal July 2007
Eelgrass Leaf Surface Microbiomes Are Locally Variable and Highly Correlated with Epibiotic Eukaryotes journal July 2017
Methylobacterium-plant interaction genes regulated by plant exudate and quorum sensing molecules journal January 2013
Biological Control in the Phyllosphere journal September 1992
Beyond Light: Physical, Geological, and Geochemical Parameters as Possible Submersed Aquatic Vegetation Habitat Requirements journal February 2001
Nitric Oxide: A Multitasked Signaling Gas in Plants journal April 2015

Cited By (4)

Advances and Challenges in Metatranscriptomic Analysis journal September 2019
Tomato RNA-seq Data Mining Reveals the Taxonomic and Functional Diversity of Root-Associated Microbiota journal December 2019
Regional and Microenvironmental Scale Characterization of the Zostera muelleri Seagrass Microbiome journal May 2019
Climate Change Impacts on Seagrass Meadows and Macroalgal Forests: An Integrative Perspective on Acclimation and Adaptation Potential journal June 2018

Figures / Tables (8)


Similar Records

Global Diversity and Biogeography of the Zostera marina Mycobiome
Journal Article · Wed May 26 00:00:00 EDT 2021 · Applied and Environmental Microbiology · OSTI ID:1628164

The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea
Journal Article · Wed Jan 27 00:00:00 EST 2016 · Nature (London) · OSTI ID:1628164

Microbiome differences in sugarcane and metabolically engineered oilcane accessions and their implications for bioenergy production
Journal Article · Thu Mar 30 00:00:00 EDT 2023 · Biotechnology for Biofuels and Bioproducts · OSTI ID:1628164