The Sphagnum microbiome: new insights from an ancient plant lineage

Peat mosses of the genus Sphagnum play a major role in global carbon storage and dominate many northern peatland ecosystems, which are currently being subjected to some of the most rapid climate changes on Earth.Arapidly expanding database indicates that a diverse community of microorganisms is inti...

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Published inThe New phytologist Vol. 211; no. 1; pp. 57 - 64
Main Authors Kostka, Joel E., Weston, David J., Glass, Jennifer B., Lilleskov, Erik A., Shaw, A. Jonathan, Turetsky, Merritt R.
Format Journal Article
LanguageEnglish
Published England New Phytologist Trust 01.07.2016
Wiley Subscription Services, Inc
Wiley
Subjects
60 APPLIED LIFE SCIENCES
Acidity
Aerobic conditions
antagonists
Bacteria
BASIC BIOLOGICAL SCIENCES
carbon
Carbon cycle
carbon sequestration
Carboxylic acids
Cations
Climate change
Community structure
Cultivation
Drought
Ecosystems
Environmental factors
Environmental research
fungi
Habitats
high-throughput nucleotide sequencing
host plants
Leaves
methanotroph
Microbial activity
microbiome
Microbiota - genetics
Microbiota - physiology
mutualism
nitrogen
Nitrogen fixation
nitrogen-fixing bacteria
Nucleic acids
Nutrient cycles
Pathogens
peatland
peatlands
Physiological ecology
plant growth promotion
Plant tissues
Polymers
prokaryotic cells
Soil types
Sphagnopsida - microbiology
Sphagnum
symbionts
Tansley insights
tissues
methanotroph
bacteria
fungi
peatland
nitrogen fixation
microbiome
plant growth promotion
Sphagnum
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Abstract Peat mosses of the genus Sphagnum play a major role in global carbon storage and dominate many northern peatland ecosystems, which are currently being subjected to some of the most rapid climate changes on Earth.Arapidly expanding database indicates that a diverse community of microorganisms is intimately associated with Sphagnum, inhabiting the tissues and surface of the plant. Here we summarize the current state of knowledge regarding the Sphagnum microbiome and provide a perspective for future research directions. Although the majority of the microbiome remains uncultivated and its metabolic capabilities uncharacterized, prokaryotes and fungi have the potential to act as mutualists, symbionts, or antagonists of Sphagnum. For example, methanotrophic and nitrogen-fixing bacteria may benefit the plant host by providing up to 20–30% of Sphagnum carbon and nitrogen, respectively. Next-generation sequencing approaches have enabled the detailed characterization of microbiome community composition in peat mosses. However, as with other ecologically or economically important plants, our knowledge of Sphagnum–microbiome associations is in its infancy. In order to attain a predictive understanding of the role of the microbiome in Sphagnum productivity and ecosystem function, the mechanisms of plant–microbiome interactions and the metabolic potential of constituent microbial populations must be revealed.
AbstractList 57 I. I. Introduction Peat mosses in the genus Sphagnum represent an ancient, early branching lineage of land plants that is largely responsible for the complex adaptive characteristics of northern peatlands (Dise, ; Shaw et al., ). Sphagnum can dominate primary productivity in northern ecosystems, including boreal forests and especially peatlands (Turetsky et al., , ). Because c. 50% of peat volume in boreal peatlands is comprised largely of Sphagnum remains (Turetsky, ), it has been said that more carbon is stored in Sphagnum than in any other genus of plant (Clymo & Hayward, ; Van Breemen, ). Sphagnum mosses are keystone species that shape their habitat through unique biochemical and morphological adaptations that together result in an acidic, permeable and nutrient-poor environment. These adaptations appear to favor Sphagnum growth relative to vascular plants (Van Breemen, ), as well as allowing Sphagnum to strongly influence ecosystem function, including the cycling of water, nutrients, energy, and carbon in northern ecosystems (Turetsky et al., ). Peatlands are thought to store one-third of Earth's soil carbon because degradation is inhibited by the acidic, nutrient-poor, cold, water-saturated and largely anoxic conditions. Sphagnum creates or at least contributes to many of these conditions. Without roots, the moss efficiently holds water in nonphotosynthetic, porous hyaline cells that can account for 80% of the plant's stem and leaf volume (Turetsky et al., ). The moss intercepts and retains nutrients efficiently through direct uptake and exchange of cations with H+, thus reducing cation availability to vascular plants, while at the same time acidifying its environment to a pH lower than most other plants can withstand (Lamers et al., ; Limpens et al., ). Sphagnum wages chemical biowarfare to outcompete other plants in its ecosystem. The decomposition of peat carbon is thought to be inhibited by antimicrobial properties of Sphagnum (Verhoeven & Liefveld, ). Biomass of the living plant consists mainly of polysaccharides made up of glucose and galacturonic acid units. Galacturonic acid is rich in carboxylic acid groups that give Sphagnum its high cation exchange capacity (Spearing, ). Acidity generally retards microbial metabolism. Sphagnum biomass is also recalcitrant or resistant to degradation as a result of other organic constituents. Although the plant lacks lignin, polyphenolic polymers termed sphagnic acid chemically protect cell wall polysaccharides from being degraded (Freeman et al., ). A pectin-like compound, sphagnan, may also suppress microbial activity by inactivating extracellular enzymes and strongly binding to nitrogen and micronutrients (Hajek et al., ). While Sphagnum manufactures an inhospitable surrounding environment, it simultaneously cultivates a diverse microbial community, or microbiome, associated with its tissues. The microbiome may be at least partially responsible for the ecological dominance of the moss. The objective of this Tansley insight is to summarize the current state of knowledge on the Sphagnum microbiome and to provide a perspective for future research directions. For the purposes of this review, we define the microbiome broadly as those microorganisms that live inside (endosphere) or on (ectosphere) living Sphagnum plants. 57 II. II. What defines the peat moss microbiome? Plant microbiome research is in its infancy. Analogous to human microbiome research a decade ago, we are still in the discovery phase, characterizing the community composition of microbiomes associated with a variety of economically and ecologically important plants. Tens of thousands of microbial species associate with plants, and plant-microbe interactions are crucial to plant health (Lundberg et al., ; Ofek-Lalzar et al., ). Microbes have the potential to benefit plants through nutrient acquisition, disease suppression, and modulation of host immunity (Mendes et al., ; Berendsen et al., ). In particular, arbuscular mycorrhizas and root nodulation are examples of symbioses with well-described benefits to plants. Until recently, characterization of plant-associated microbial communities was hampered by methodologies lacking phylogenetic resolution and sequencing depth. The development and availability of next-generation sequencing technologies have facilitated rapid advances in the field. In order to define the microbiome, one first has to confirm the identity and genotype of the plant host. Sphagnum plants provide additional challenges in this area because of an unresolved phylogeny (Shaw et al., ). Moreover, as for many plant hosts, the definition of what is plant-associated has varied in previous studies of the Sphagnum microbiome. Viewpoints on what is 'Sphagnum-associated' range from microbes of the bulk peat in the surface layer of peatlands where active photosynthesis occurs (Putkinen et al., ) to those associated with the living vegetative part of the plant (gametophyte) along with associated soil (Raghoebarsing et al., ). As we strive to establish the structure-function relationships of the microbiome that benefit the plant host, there is a need to verify the taxonomy of Sphagnum individuals using genotyping methods in parallel with morphological taxonomy and microbiome interrogation. Sphagnum microbiomes are hypothesized to differ from those of most host plants because mosses have no roots and hence microbial inhabitants are mainly detected in the hyaline cells of leaf tissues (Fig. ; Bragina et al., ). The water-filled hyaline cells, or hyalocytes, are dead, hollow and often pore-containing cells in the leaves, stems and branches of the gametophyte. Hyaline cells allow for storage of water as well as the exchange of water between these cells and adjacent photosynthetic cells. Chlorophyllose cells were thus far shown to contain few to no bacteria. With an elevated pH, hyaline cells could act as 'oases' for microbes in the acidic peatland pore water. One could imagine these hyalocytes as tiny chemostats that cultivate microbes, which in turn benefit the peat moss host. Plants are thought to contain a 'core microbiome' that consists of microbial taxa that are common to plant species or habitat (Vandenkoornhuyse et al., ). The diversity and function of microbial groups that comprise the microbiome have been shown in model plants such as Arabidopsis to be specific to soil type or plant genotype (Lundberg et al., ) as well as to correlate with plant fitness or health (Kembel et al., ). However, for most plants, the microbiome has not been characterized in sufficient detail to resolve differences between plant species or functional traits. Metagenomic studies foster hypotheses on how specific microbially catalyzed functions may be linked to plant fitness, including studies of Sphagnum (Bragina et al., ). However, further research is needed to determine the role of specific microbial groups in plant health at the ecosystem scale. 58 III. III. Structure and function of the Sphagnum microbiome The majority of cultivation-independent molecular studies of Sphagnum microbiomes to date have targeted small subunit ribosomal RNA (SSU rRNA) genes or functional genes of prokaryotes extracted from unwashed gametophytes (Bragina et al., , ). Microbial cells were often separated from homogenized plant biomass using a centrifugation method. Evidence at this time points to a predominance and high diversity of Bacteria in the microbiome, with few to no members of the Archaea detected (Bragina et al., ). Of the Bacteria, members of the Proteobacteria and Acidobacteria phyla are by far the most abundant, comprising the majority of SSU rRNA gene sequences obtained, with a lower relative abundance of other taxa (Bacteroidetes, Cyanobacteria, Planctomycetes, Verrucomicrobia, Actinobacteria) (Bragina et al., ; Lin et al., ,b). The ecological factors controlling microbiome structure and function are just beginning to be explored. A fairly large body of research suggests that microbiome community composition is distinct to the Sphagnum host species, and evidence points to environmental factors such as pH and nutrient availability as ecological drivers of microbiome community structure (Opelt et al., ; Bragina et al., ; Jassey et al., ; Leppaenen et al., ). However, other studies challenge this view, showing that microbiome composition does not vary significantly between different peat moss species (Bragina et al., ; Putkinen et al., ). Further studies are needed at the ecosystem scale to understand the role of the environment vs plant host in the population dynamics of Sphagnum microbiomes. As already described, Sphagnum-dominated peatlands represent extreme habitats for microbial life, as the prevailing conditions are acidic, cold, nutrient-poor, water-saturated and therefore anoxic below the surface. These conditions are believed to inhibit microbial metabolism, leading to carbon storage. These extreme conditions also mean that the constituent microorganisms tend to be slow-growing, oligotrophic and more difficult to obtain in pure culture. As demonstrated by cultivation-independent studies, Sphagnum microbiomes contain a large diversity of as yet uncultivated bacteria with unknown physiologies (Dedysh, ; Leppaenen et al., ; Lin et al., ,b). Cultivation work has largely focused on microorganisms isolated from bulk peat or those from gametophytes along with adhered soil, and a few studies have used surface sterilization to select for endophytes. Dedysh () provided a comprehensive review of microbes that have been cultivated from bulk peat, many of which have also been detected using molecular techniques in the Sphagnum microbiome. Bacterial isolates from the ectosphere or endosphere of Sphagnum tissues have demonstrated the potential for a number of plant growth promotion capabilities, including nutrient acquisition, antagonism toward fungal or bacterial plant pathogens, and production of plant hormones (Table ;
Peat mosses of the genus Sphagnum play a major role in global carbon storage and dominate many northern peatland ecosystems, which are currently being subjected to some of the most rapid climate changes on Earth. A rapidly expanding database indicates that a diverse community of microorganisms is intimately associated with Sphagnum, inhabiting the tissues and surface of the plant. Here we summarize the current state of knowledge regarding the Sphagnum microbiome and provide a perspective for future research directions. Although the majority of the microbiome remains uncultivated and its metabolic capabilities uncharacterized, prokaryotes and fungi have the potential to act as mutualists, symbionts, or antagonists of Sphagnum. For example, methanotrophic and nitrogen-fixing bacteria may benefit the plant host by providing up to 20-30% of Sphagnum carbon and nitrogen, respectively. Next-generation sequencing approaches have enabled the detailed characterization of microbiome community composition in peat mosses. However, as with other ecologically or economically important plants, our knowledge of Sphagnum-microbiome associations is in its infancy. In order to attain a predictive understanding of the role of the microbiome in Sphagnum productivity and ecosystem function, the mechanisms of plant-microbiome interactions and the metabolic potential of constituent microbial populations must be revealed.
57 I. 57 II. 58 III. 59 IV. 59 V. 61 VI. 62 63 References 63 SUMMARY: Peat mosses of the genus Sphagnum play a major role in global carbon storage and dominate many northern peatland ecosystems, which are currently being subjected to some of the most rapid climate changes on Earth. A rapidly expanding database indicates that a diverse community of microorganisms is intimately associated with Sphagnum, inhabiting the tissues and surface of the plant. Here we summarize the current state of knowledge regarding the Sphagnum microbiome and provide a perspective for future research directions. Although the majority of the microbiome remains uncultivated and its metabolic capabilities uncharacterized, prokaryotes and fungi have the potential to act as mutualists, symbionts, or antagonists of Sphagnum. For example, methanotrophic and nitrogen‐fixing bacteria may benefit the plant host by providing up to 20–30% of Sphagnum carbon and nitrogen, respectively. Next‐generation sequencing approaches have enabled the detailed characterization of microbiome community composition in peat mosses. However, as with other ecologically or economically important plants, our knowledge of Sphagnum–microbiome associations is in its infancy. In order to attain a predictive understanding of the role of the microbiome in Sphagnum productivity and ecosystem function, the mechanisms of plant–microbiome interactions and the metabolic potential of constituent microbial populations must be revealed.
57 I. 57 II. 58 III. 59 IV. 59 V. 61 VI. 62 63 References 63 Summary Peat mosses of the genus Sphagnum play a major role in global carbon storage and dominate many northern peatland ecosystems, which are currently being subjected to some of the most rapid climate changes on Earth. A rapidly expanding database indicates that a diverse community of microorganisms is intimately associated with Sphagnum, inhabiting the tissues and surface of the plant. Here we summarize the current state of knowledge regarding the Sphagnum microbiome and provide a perspective for future research directions. Although the majority of the microbiome remains uncultivated and its metabolic capabilities uncharacterized, prokaryotes and fungi have the potential to act as mutualists, symbionts, or antagonists of Sphagnum. For example, methanotrophic and nitrogen‐fixing bacteria may benefit the plant host by providing up to 20–30% of Sphagnum carbon and nitrogen, respectively. Next‐generation sequencing approaches have enabled the detailed characterization of microbiome community composition in peat mosses. However, as with other ecologically or economically important plants, our knowledge of Sphagnum–microbiome associations is in its infancy. In order to attain a predictive understanding of the role of the microbiome in Sphagnum productivity and ecosystem function, the mechanisms of plant–microbiome interactions and the metabolic potential of constituent microbial populations must be revealed.
Peat mosses of the genus Sphagnum play a major role in global carbon storage and dominate many northern peatland ecosystems, which are currently being subjected to some of the most rapid climate changes on Earth. A rapidly expanding database indicates that a diverse community of microorganisms is intimately associated with Sphagnum , inhabiting the tissues and surface of the plant. Here we summarize the current state of knowledge regarding the Sphagnum microbiome and provide a perspective for future research directions. Although the majority of the microbiome remains uncultivated and its metabolic capabilities uncharacterized, prokaryotes and fungi have the potential to act as mutualists, symbionts, or antagonists of Sphagnum . For example, methanotrophic and nitrogen‐fixing bacteria may benefit the plant host by providing up to 20–30% of Sphagnum carbon and nitrogen, respectively. Next‐generation sequencing approaches have enabled the detailed characterization of microbiome community composition in peat mosses. However, as with other ecologically or economically important plants, our knowledge of Sphagnum –microbiome associations is in its infancy. In order to attain a predictive understanding of the role of the microbiome in Sphagnum productivity and ecosystem function, the mechanisms of plant–microbiome interactions and the metabolic potential of constituent microbial populations must be revealed. Contents Summary 57 I. Introduction 57 II. What defines the peat moss microbiome? 58 III. Structure and function of the Sphagnum microbiome 59 IV. Functional guilds of microbes that benefit Sphagnum 59 V. Fungi in the Sphagnum microbiome 61 VI. Conclusions and future directions 62 Acknowledgements 63 References 63
Here, peat mosses of the genus Sphagnum play a major role in global carbon storage and dominate many northern peatland ecosystems, which are currently being subjected to some of the most rapid climate changes on Earth. A rapidly expanding database indicates that a diverse community of microorganisms is intimately associated with Sphagnum, inhabiting the tissues and surface of the plant. Here we summarize the current state of knowledge regarding the Sphagnum microbiome and provide a perspective for future research directions. Although the majority of the microbiome remains uncultivated and its metabolic capabilities uncharacterized, prokaryotes and fungi have the potential to act as mutualists, symbionts, or antagonists of Sphagnum. For example, methanotrophic and nitrogen-fixing bacteria may benefit the plant host by providing up to 20–30% of Sphagnum carbon and nitrogen, respectively. Next-generation sequencing approaches have enabled the detailed characterization of microbiome community composition in peat mosses. However, as with other ecologically or economically important plants, our knowledge of Sphagnum–microbiome associations is in its infancy. In order to attain a predictive understanding of the role of the microbiome in Sphagnum productivity and ecosystem function, the mechanisms of plant–microbiome interactions and the metabolic potential of constituent microbial populations must be revealed.
Peat mosses of the genus Sphagnum play a major role in global carbon storage and dominate many northern peatland ecosystems, which are currently being subjected to some of the most rapid climate changes on Earth.Arapidly expanding database indicates that a diverse community of microorganisms is intimately associated with Sphagnum, inhabiting the tissues and surface of the plant. Here we summarize the current state of knowledge regarding the Sphagnum microbiome and provide a perspective for future research directions. Although the majority of the microbiome remains uncultivated and its metabolic capabilities uncharacterized, prokaryotes and fungi have the potential to act as mutualists, symbionts, or antagonists of Sphagnum. For example, methanotrophic and nitrogen-fixing bacteria may benefit the plant host by providing up to 20–30% of Sphagnum carbon and nitrogen, respectively. Next-generation sequencing approaches have enabled the detailed characterization of microbiome community composition in peat mosses. However, as with other ecologically or economically important plants, our knowledge of Sphagnum–microbiome associations is in its infancy. In order to attain a predictive understanding of the role of the microbiome in Sphagnum productivity and ecosystem function, the mechanisms of plant–microbiome interactions and the metabolic potential of constituent microbial populations must be revealed.
Author A. Jonathan Shaw
David J. Weston
Merritt R. Turetsky
Erik A. Lilleskov
Jennifer B. Glass
Joel E. Kostka
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  organization: Georgia Institute of Technology
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  surname: Weston
  fullname: Weston, David J.
  organization: Oak Ridge National Lab
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  givenname: Jennifer B.
  surname: Glass
  fullname: Glass, Jennifer B.
  organization: Georgia Institute of Technology
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  givenname: Erik A.
  surname: Lilleskov
  fullname: Lilleskov, Erik A.
  organization: USDA Forest Service
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  givenname: A. Jonathan
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  fullname: Shaw, A. Jonathan
  organization: Duke University
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  givenname: Merritt R.
  surname: Turetsky
  fullname: Turetsky, Merritt R.
  organization: University of Guelph
BackLink https://www.ncbi.nlm.nih.gov/pubmed/27173909$$D View this record in MEDLINE/PubMed
https://www.osti.gov/servlets/purl/1356904$$D View this record in Osti.gov
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Issue 1
Keywords methanotroph
bacteria
fungi
peatland
nitrogen fixation
microbiome
plant growth promotion
Sphagnum
Language English
License http://onlinelibrary.wiley.com/termsAndConditions#am
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2016 The Authors. New Phytologist © 2016 New Phytologist Trust.
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Snippet Peat mosses of the genus Sphagnum play a major role in global carbon storage and dominate many northern peatland ecosystems, which are currently being...
57 I. 57 II. 58 III. 59 IV. 59 V. 61 VI. 62 63 References 63 Summary Peat mosses of the genus Sphagnum play a major role in global carbon storage and dominate...
Peat mosses of the genus Sphagnum play a major role in global carbon storage and dominate many northern peatland ecosystems, which are currently being...
57 I. 57 II. 58 III. 59 IV. 59 V. 61 VI. 62 63 References 63 SUMMARY: Peat mosses of the genus Sphagnum play a major role in global carbon storage and dominate...
57 I. I. Introduction Peat mosses in the genus Sphagnum represent an ancient, early branching lineage of land plants that is largely responsible for the...
Here, peat mosses of the genus Sphagnum play a major role in global carbon storage and dominate many northern peatland ecosystems, which are currently being...
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SubjectTerms 60 APPLIED LIFE SCIENCES
Acidity
Aerobic conditions
antagonists
Bacteria
BASIC BIOLOGICAL SCIENCES
carbon
Carbon cycle
carbon sequestration
Carboxylic acids
Cations
Climate change
Community structure
Cultivation
Drought
Ecosystems
Environmental factors
Environmental research
fungi
Habitats
high-throughput nucleotide sequencing
host plants
Leaves
methanotroph
Microbial activity
microbiome
Microbiota - genetics
Microbiota - physiology
mutualism
nitrogen
Nitrogen fixation
nitrogen-fixing bacteria
Nucleic acids
Nutrient cycles
Pathogens
peatland
peatlands
Physiological ecology
plant growth promotion
Plant tissues
Polymers
prokaryotic cells
Soil types
Sphagnopsida - microbiology
Sphagnum
symbionts
Tansley insights
tissues
Title The Sphagnum microbiome: new insights from an ancient plant lineage
URI https://www.jstor.org/stable/newphytologist.211.1.57
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fnph.13993
https://www.ncbi.nlm.nih.gov/pubmed/27173909
https://www.proquest.com/docview/1792495965
https://www.proquest.com/docview/1793216413
https://www.proquest.com/docview/1808717035
https://www.proquest.com/docview/2000161433
https://www.osti.gov/servlets/purl/1356904
Volume 211
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