Microbes are the unseen majority in soil and comprise a large portion of lifes genetic diversity. Despite their abundance, the impact of soil microbes on ecosystem processes is still poorly understood. Here we explore the various roles that soil microbes play in terrestrial ecosystems with special emphasis on their contribution to plant productivity and diversity. Soil microbes are important regulators of plant productivity, especially in nutrient poor ecosystems where plant symbionts are responsible for the acquisition of limiting nutrients. Mycorrhizal fungi and nitrogenfixing bacteria are responsible for c. 5‐20% (grassland and savannah) to 80% (temperate and boreal forests) of all nitrogen, and up to 75% of phosphorus, that is acquired by plants annually. Free-living microbes also strongly regulate plant productivity, through the mineralization of, and competition for, nutrients that sustain plant productivity. Soil microbes, including microbial pathogens, are also important regulators of plant community dynamics and plant diversity, determining plant abundance and, in some cases, facilitating invasion by exotic plants. Conservative estimates suggest that c. 20 000 plant species are completely dependent on microbial symbionts for growth and survival pointing to the importance of soil microbes as regulators of plant species richness on Earth. Overall, this review shows that soil microbes must be considered as important drivers of plant diversity and productivity in terrestrial ecosystems.

/pdf/the-unseen-majority-soil-microbes-as-drivers-of-plant-1yjo7xbywu.pdf

The unseen majority: Soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems

The colonization of land by plants appears to have coincided with the appearance of mycorrhiza-like fungi. Over evolutionary time, fungi have maintained their prominent role in the formation of mycorrhizal associations. In addition, however, they have been able to occupy other terrestrial niches of which the decomposition of recalcitrant organic matter is perhaps the most remarkable. This implies that, in contrast to that of aquatic organic matter decomposition, bacteria have not been able to monopolize decomposition processes in terrestrial ecosystems. The emergence of fungi in terrestrial ecosystems must have had a strong impact on the evolution of terrestrial bacteria. On the one hand, potential decomposition niches, e.g. lignin degradation, have been lost for bacteria, whereas on the other hand the presence of fungi has itself created new bacterial niches. Confrontation between bacteria and fungi is ongoing, and from studying contemporary interactions, we can learn about the impact that fungi presently have, and have had in the past, on the ecology and evolution of terrestrial bacteria. In the first part of this review, the focus is on niche differentiation between soil bacteria and fungi involved in the decomposition of plant-derived organic matter. Bacteria and fungi are seen to compete for simple plant-derived substrates and have developed antagonistic strategies. For more recalcitrant organic substrates, e.g. cellulose and lignin, both competitive and mutualistic strategies appear to have evolved. In the second part of the review, bacterial niches with respect to the utilization of fungal-derived substrates are considered. Here, several lines of development can be recognized, ranging from mutualistic exudate-consuming bacteria that are associated with fungal surfaces to endosymbiotic and mycophagous bacteria. In some cases, there are indications of fungal specific selection in fungus-associated bacteria, and possible mechanisms for such selection are discussed.

Living in a fungal world: impact of fungi on soil bacterial niche development⋆

Plant growth promoting bacteria (PGPR) associations range in degree of bacterial proximity to the root and intimacy of association. In general, these can be separated into extracellular PGPR (ePGPR), existing in the rhizosphere, on the rhizoplane or in the spaces between cells of the root cortex, and intracellular PGPR (iPGPR), which exist inside root cells, generally in specialized nodular structures. The latter includes rhizobia and Frankia species, both of which fix nitrogen in symbiosis with higher plants. There has been considerable development in understanding signaling mechanisms of rhizobia (iPGPR) during the establishment of the rhizobia–legume symbiosis, and this may serve as a model of knowledge regarding cross-talk and plant growth promoting mechanisms. We provide a detailed review of this process, including plant-to-bacteria signal molecules, followed by bacterial perception and consequent production of bacteria-to-plant signals. A history of PGPR discovery is also provided, indicating progress in understanding each of the PGPR groups. Recent advances in understanding plant growth responses to microbial signals are reviewed, along with the research areas that require attention. Based on new understandings of signaling mechanisms in the iPGPR (rhizobia) and recent findings with ePGPR we are able to speculate regarding general patterns of signaling in the ePGPR.

Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes

Nitrogen is generally considered one of the major limiting nutrients in plant growth. The biological process responsible for reduction of molecular nitrogen into ammonia is referred to as nitrogen fixation. A wide diversity of nitrogen-fixing bacterial species belonging to most phyla of the Bacteria domain have the capacity to colonize the rhizosphere and to interact with plants. Leguminous and actinorhizal plants can obtain their nitrogen by association with rhizobia or Frankia via differentiation on their respective host plants of a specialized organ, the root nodule. Other symbiotic associations involve heterocystous cyanobacteria, while increasing numbers of nitrogen-fixing species have been identified as colonizing the root surface and, in some cases, the root interior of a variety of cereal crops and pasture grasses. Basic and advanced aspects of these associations are covered in this review.

/pdf/nitrogen-fixing-bacteria-associated-with-leguminous-and-non-1gzxmeeigu.pdf

Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants

Biological nitrogen fixation in non-legume plants

Summary 449

I. INTRODUCTION 450

II. THE PARTNERS 451

1. Cyanobionts and their role 451

2. Hosts and their role 453

3. Location of cyanobionts in their hosts 455

III. INITIATION AND DEVELOPMENT OF SYMBIOSES 458

1. Initiation of symbioses 458

2. Geosiphon pyriforme 458

3. Cyanolichens 459

4. Liverworts and hornworts 460

5. Azolla 460

6. Cycads 461

7. Gunnera 461

IV. THE SYMBIOSES 462

1. Geographical distribution and ecological significance 462

2. Benefits to the partners 462

(a) Benefits to the cyanobionts 462

(b) Benefits to the hosts 463

3. Duration and stability 463

4. Mode of transmission and perpetuation 463

5. Recognition between the partners 464

6. Specificity and diversity 464

7. Symbiosis-related genes 465

8. Modifications of the cyanobiont 466

(a) Growth and morphology 466

(b) Photosynthesis and carbon metabolism 467

(c) Glutamine synthetase 467

(d) Heterocysts 469

(e) N2fixation 470

9. Nutrient exchange 471

(a) Carbon 471

(b) Nitrogen 472

V. EVOLUTIONARY ASPECTS 472

VI. ARTIFICIAL SYMBIOSES 474

VII. FUTURE OUTLOOK AND PERSPECTIVES 475

1. Cryptic symbioses 476

2. Developmental profile of symbiotic tissues 476

3. Sensing and signalling 476

4. Genetic aspects 476

5. Physiological and biochemical aspects of nutrient exchange 477

6. Microaerobiosis 477

7. Potential applications 477

Acknowledgements 477

References 477

Cyanobacteria are an ancient, morphologically diverse group of prokaryotes with an oxygenic photosynthesis. Many cyanobacteria also possess the ability to fix N2. Although well suited to an independent existence in nature, some cyanobacteria occur in symbiosis with a wide range of hosts (protists, animals and plants). Among plants, such symbioses have independently evolved in phylogenetically diverse genera belonging to the algae, fungi, bryophytes, pteridophytes, gymnosperms and angiosperms. These are N2-fixing symbioses involving heterocystous cyanobacteria, particularly Nostoc, as cyanobionts (cyanobacterial partners). A given host species associates with only a particular cyanobiont genus but such specificity does not extend to the strain level. The cyanobiont is located under a microaerobic environment in a variety of host organs and tissues (bladder, thalli and cephalodia in fungi; cavities in gametophytes of hornworts and liverworts or fronds of the Azolla sporophyte; coralloid roots in cycads; stem glands in Gunnera). Except for fungi, the hosts form these structures ahead of the cyanobiont infection. The symbiosis lasts for one generation except in Azolla and diatoms, in which it is perpetuated from generation to generation. Within each generation, multiple fresh infections occur as new symbiotic tissues and organs develop. The symbioses are stable over a wide range of environmental conditions, and sensing–signalling between partners ensures their synchronized growth and development. The cyanobiont population is kept constant in relation to the host biomass through controlled initiation and infection, nutrient supply and cell division. In most cases, the partners have remained facultative, with the cyanobiont residing extracellularly in the host. However, in the water-fern Azolla and the freshwater diatom Rhopalodia the association is obligate. The cyanobionts occur intracellularly in diatoms, the fungus Geosiphon and the angiosperm Gunner a. Close cell–cell contact and the development of special structures ensure efficient nutrient exchange between the partners. The mobile nutrients are normal products of the donor cells, although their production is increased in symbiosis. Establishment of cyanobacterial–plant symbioses differs from chloroplast evolution. In these symbioses, the cyanobiont undergoes structural–functional changes suited to its role as provider of fixed N rather than fixed C, and the level of intimacy is far less than that of an organelle. This review provides an updated account of cyanobacterial–plant symbioses, particularly concerning developments during the past 10 yr. Various aspects of these symbioses such as initiation and development, symbiont diversity, recognition and signalling, structural–functional modifications, integration, and nutrient exchange are reviewed and discussed, as are evolutionary aspects and the potential uses of cyanobacterial–plant symbioses. Finally we outline areas that require special attention for future research. Not only will these provide information of academic interest but they will also help to improve the use of Azolla as green manure, to enable us to establish artificial N2-fixing associations with cereals such as rice, and to allow the manipulation of free-living cyanobacteria for photobiological ammonia or hydrogen production or for use as biofertilizers.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1046/j.1469-8137.2000.00720.x

E. Söderbäck

Papers

Tansley Review No. 116: Cyanobacterium-plant symbioses.

Cyanobacterial-plant symbioses

Immunogold localization of hydrogenase in the cyanobacterial-plant symbioses Peltigera canina, Anthoceros punctatus and Gunnera magellanica