Availability of carbon and nitrogen in soil affects Metarhizium robertsii root colonization and transfer of insect-derived nitrogen

Larissa Barelli; Scott W Behie; Michael J Bidochka

doi:10.1093/femsec/fiz144

Availability of carbon and nitrogen in soil affects Metarhizium robertsii root colonization and transfer of insect-derived nitrogen

FEMS Microbiology Ecology ◽

10.1093/femsec/fiz144 ◽

2019 ◽

Vol 95 (10) ◽

Author(s):

Larissa Barelli ◽

Scott W Behie ◽

Michael J Bidochka

Keyword(s):

Ammonium Nitrate ◽

Root Colonization ◽

Pathogenic Fungus ◽

Broth Culture ◽

Nitrogen Transfer ◽

Symbiotic Association ◽

Metarhizium Robertsii ◽

Carbon And Nitrogen ◽

Ecological Importance ◽

Fungal Gene Expression

ABSTRACT The endophytic, insect pathogenic fungus, Metarhizium, exchanges insect-derived nitrogen for photosynthate as part of a symbiotic association similar to well-known mycorrhizal relationships. However, little is known about this nitrogen transfer in soils where there is an abundance of nitrogen and/or carbon. Here, we applied D-glucose and ammonium nitrate to soil to examine the effect on root colonization and transfer of labelled nitrogen (15N) from an insect (injected with 15N-ammonium sulfate) to Metarhizium robertsii, into leaves of the common bean, Phaseolus vulgaris, over the course of 28 days. Application of exogenous carbon and/or nitrogen to soils significantly reduced detectable 15N in plant leaves. Metarhizium root colonization, quantified with real-time PCR, revealed colonization persisted under all conditions but was significantly greater on roots in soil supplemented with glucose and significantly lower in soil supplemented with ammonium nitrate. Fungal gene expression analysis revealed differential expression of sugar and nitrogen transporters (mrt, st3, nrr1, nit1, mep2) when Metarhizium was grown in pure broth culture or in co-culture with plant roots under various carbon and nitrogen conditions. The observation that Metarhizium maintained root colonization in the absence of nitrogen transfer, and without evidence of plant harm, is intriguing and indicates additional benefits with ecological importance.

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Ubiquity of Insect-Derived Nitrogen Transfer to Plants by Endophytic Insect-Pathogenic Fungi: an Additional Branch of the Soil Nitrogen Cycle

Applied and Environmental Microbiology ◽

10.1128/aem.03338-13 ◽

2013 ◽

Vol 80 (5) ◽

pp. 1553-1560 ◽

Cited By ~ 88

Author(s):

Scott W. Behie ◽

Michael J. Bidochka

Keyword(s):

Panicum Virgatum ◽

Pathogenic Fungus ◽

Insect Herbivory ◽

Pathogenic Fungi ◽

Nitrogen Transfer ◽

Metarhizium Robertsii ◽

Content Type ◽

Lecanicillium Lecanii ◽

Worldwide Distribution ◽

Insect Pathogenic Fungi

ABSTRACTThe study of symbiotic nitrogen transfer in soil has largely focused on nitrogen-fixing bacteria. Vascular plants can lose a substantial amount of their nitrogen through insect herbivory. Previously, we showed that plants were able to reacquire nitrogen from insects through a partnership with the endophytic, insect-pathogenic fungusMetarhizium robertsii. That is, the endophytic capability and insect pathogenicity ofM. robertsiiare coupled so that the fungus acts as a conduit to provide insect-derived nitrogen to plant hosts. Here, we assess the ubiquity of this nitrogen transfer in fiveMetarhiziumspecies representing those with broad (M. robertsii,M. brunneum, andM. guizhouense) and narrower insect host ranges (M. acridumandM. flavoviride), as well as the insect-pathogenic fungiBeauveria bassianaandLecanicillium lecanii. Insects were injected with15N-labeled nitrogen, and we tracked the incorporation of15N into two dicots, haricot bean (Phaseolus vulgaris) and soybean (Glycine max), and two monocots, switchgrass (Panicum virgatum) and wheat (Triticum aestivum), in the presence of these fungi in soil microcosms. AllMetarhiziumspecies andB. bassianabut notL. lecaniishowed the capacity to transfer nitrogen to plants, although to various degrees. Endophytic association by these fungi increased overall plant productivity. We also showed that in the field, where microbial competition is potentially high,M. robertsiiwas able to transfer insect-derived nitrogen to plants.Metarhiziumspp. andB. bassianahave a worldwide distribution with high soil abundance and may play an important role in the ecological cycling of insect nitrogen back to plant communities.

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Carbon and nitrogen transfer in leaf litter mixtures

Soil Biology and Biochemistry ◽

10.1016/j.soilbio.2012.09.015 ◽

2013 ◽

Vol 57 ◽

pp. 341-348 ◽

Cited By ~ 28

Author(s):

S. Linnea Berglund ◽

Göran I. Ågren ◽

Alf Ekblad

Keyword(s):

Leaf Litter ◽

Nitrogen Transfer ◽

Carbon And Nitrogen ◽

Litter Mixtures

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Three sympatrically occurring species of Metarhizium show plant rhizosphere specificity

Microbiology ◽

10.1099/mic.0.051102-0 ◽

2011 ◽

Vol 157 (10) ◽

pp. 2904-2911 ◽

Cited By ~ 88

Author(s):

Michael Wyrebek ◽

Cristina Huber ◽

Ramanpreet Kaur Sasan ◽

Michael J. Bidochka

Keyword(s):

Tree Species ◽

Acer Saccharum ◽

Panicum Virgatum ◽

Sugar Maple ◽

Root Exudate ◽

Pathogenic Fungus ◽

Plant Roots ◽

Metarhizium Robertsii ◽

Grass Roots

Here we tested the hypothesis that species of the soil-inhabiting insect-pathogenic fungus Metarhizium are not randomly distributed in soils but show plant-rhizosphere-specific associations. We isolated Metarhizium from plant roots at two sites in Ontario, Canada, sequenced the 5′ EF-1α gene to discern Metarhizium species, and developed an RFLP test for rapid species identification. Results indicated a non-random association of three Metarhizium species (Metarhizium robertsii, Metarhizium brunneum and Metarhizium guizhouense) with the rhizosphere of certain types of plant species (identified to species and categorized as grasses, wildflowers, shrubs and trees). M. robertsii was the only species that was found associated with grass roots, suggesting a possible exclusion of M. brunneum and M. guizhouense. Supporting this, in vitro experiments showed that M. robertsii conidia germinated significantly better in Panicum virgatum (switchgrass) root exudate than did M. brunneum or M. guizhouense. M. guizhouense and M. brunneum only associated with wildflower rhizosphere when co-occurring with M. robertsii. With the exception of these co-occurrences, M. guizhouense was found to associate exclusively with the rhizosphere of tree species, predominantly Acer saccharum (sugar maple), while M. brunneum was found to associate exclusively with the rhizosphere of shrubs and trees. These associations demonstrate that different species of Metarhizium associate with specific plant types.

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Flexibility of nutritional strategies within a mutualism: food availability affects algal symbiont productivity in two congeneric sea anemone species

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2020.1860 ◽

2020 ◽

Vol 287 (1940) ◽

pp. 20201860

Author(s):

Samuel A. Bedgood ◽

Sarah E. Mastroni ◽

Matthew E. S. Bracken

Keyword(s):

Food Availability ◽

Sea Anemone ◽

Symbiotic Association ◽

Sea Anemones ◽

External Resources ◽

Carbon And Nitrogen ◽

Algal Symbionts ◽

Algal Symbiont ◽

Nutritional Strategy ◽

Nutritional Strategies

Mutualistic symbioses are common, especially in nutrient-poor environments where an association between hosts and symbionts can allow the symbiotic partners to persist and collectively out-compete non-symbiotic species. Usually these mutualisms are built on an intimate transfer of energy and nutrients (e.g. carbon and nitrogen) between host and symbiont. However, resource availability is not consistent, and the benefit of the symbiotic association can depend on the availability of resources to mutualists. We manipulated the diets of two temperate sea anemone species in the genus Anthopleura in the field and recorded the responses of sea anemones and algal symbionts in the family Symbiodiniaceae to our treatments. Algal symbiont density, symbiont volume and photosynthetic efficiency of symbionts responded to changes in sea anemone diet, but the responses depended on the species of sea anemone. We suggest that temperate sea anemones and their symbionts can respond to changes in anemone diet, modifying the balance between heterotrophy and autotrophy in the symbiosis. Our data support the hypothesis that symbionts are upregulated or downregulated based on food availability, allowing for a flexible nutritional strategy based on external resources.

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Factors involved in the amelioration of retarded symbiosis in Tinaroo glycine

Australian Journal of Agricultural Research ◽

10.1071/ar9740577 ◽

1974 ◽

Vol 25 (4) ◽

pp. 577 ◽

Cited By ~ 5

Author(s):

A Diatloff

Keyword(s):

Nitrogen Fixation ◽

Ammonium Nitrate ◽

Root Nodules ◽

Host Cells ◽

Starch Accumulation ◽

Nodule Formation ◽

Carbon And Nitrogen ◽

Slow Development ◽

Structural Differences ◽

Envelope Membranes

Root nodules formed on Tinaroo glycine (Glycine wightii) were slow to pigment and begin fixing nitrogen. Various carbon and nitrogen compounds enhanced nodule pigmentation, the greening of the plants, and the rate of nitrogen fixation at 42 days. Of these inositol, glucose, ammonium nitrate (as both foliar and root applications) and coconut milk were most effective. Riboflavin, sodium glutamate and nodule infusion had little effect. There were no structural differences between nodules enhanced respectively by glucose and ammonium nitrate. Nodules on control plants showed slow development of the bacteroids and envelope membranes, with copious starch accumulation in uninvaded host cells. It was concluded that the retarded symbiosis in formed nodules was due initially to tardy nodule formation depleting the nitrogen reserves in the seeds before nitrogen fixation began. Because of the interaction of photosynthesis and nitrogen fixation, self-regeneration of nitrogen fixation in chlorotic plants was slow without an external stimulus. It is suggested that by selecting lines of the legume with larger seeds or by incorporating nitrogen in seed pellets the problem might be overcome.

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Algal-fungal symbiosis leads to photosynthetic mycelium

eLife ◽

10.7554/elife.47815 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 16

Author(s):

Zhi-Yan Du ◽

Krzysztof Zienkiewicz ◽

Natalie Vande Pol ◽

Nathaniel E Ostrom ◽

Christoph Benning ◽

...

Keyword(s):

Physical Contact ◽

Biofuel Production ◽

Nitrogen Transfer ◽

Free Living ◽

Important Species ◽

Carbon And Nitrogen ◽

Isotope Tracer ◽

Fungal Symbiosis ◽

Mortierella Elongata ◽

Tracer Experiments

Mutualistic interactions between free-living algae and fungi are widespread in nature and are hypothesized to have facilitated the evolution of land plants and lichens. In all known algal-fungal mutualisms, including lichens, algal cells remain external to fungal cells. Here, we report on an algal–fungal interaction in which Nannochloropsis oceanica algal cells become internalized within the hyphae of the fungus Mortierella elongata. This apparent symbiosis begins with close physical contact and nutrient exchange, including carbon and nitrogen transfer between fungal and algal cells as demonstrated by isotope tracer experiments. This mutualism appears to be stable, as both partners remain physiologically active over months of co-cultivation, leading to the eventual internalization of photosynthetic algal cells, which persist to function, grow and divide within fungal hyphae. Nannochloropsis and Mortierella are biotechnologically important species for lipids and biofuel production, with available genomes and molecular tool kits. Based on the current observations, they provide unique opportunities for studying fungal-algal mutualisms including mechanisms leading to endosymbiosis.

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Description of bacteria able to degrade isoquinoline in pure culture

Canadian Journal of Microbiology ◽

10.1139/m94-089 ◽

1994 ◽

Vol 40 (7) ◽

pp. 555-560 ◽

Cited By ~ 6

Author(s):

J. Aislabie ◽

N. K. Richards ◽

T. C. Lyttle

Keyword(s):

Heterocyclic Compound ◽

Pure Culture ◽

Sole Source ◽

Broth Culture ◽

Gram Negative ◽

Carbon And Nitrogen ◽

The Family ◽

Nitrogen Heterocyclic

Isoquinoline is a nitrogen heterocyclic compound that is associated with coal- and oil-derived wastes. Four strains of bacteria able to degrade isoquinoline in pure culture were isolated from sites known to be contaminated with oil. Isoquinoline was used as the sole source of carbon and nitrogen by these isolates. Isoquinoline was initially transformed to 1-hydroxyisoquinoline, which accumulated in the broth culture, and then disappeared. The four strains isolated were Gram negative, aerobic, rod-shaped bacteria with polar flagella. The strains have been presumptively identified as members of the family Comamonadaceae.Key words: isoquinoline degradation, Comamonadaceae.not available

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Metarhizium robertsii Produces an Extracellular Invertase (MrINV) That Plays a Pivotal Role in Rhizospheric Interactions and Root Colonization

PLoS ONE ◽

10.1371/journal.pone.0078118 ◽

2013 ◽

Vol 8 (10) ◽

pp. e78118 ◽

Cited By ~ 23

Author(s):

Xinggang Liao ◽

Weiguo Fang ◽

Liangcai Lin ◽

Hsiao-Ling Lu ◽

Raymond J. St. Leger

Keyword(s):

Root Colonization ◽

Pivotal Role ◽

Metarhizium Robertsii ◽

Extracellular Invertase

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EFFECTS OF VESICULAR-ARBUSCULAR MYCORRHIZA ON 14C AND 15N DISTRIBUTION IN NODULATED FABABEANS

Canadian Journal of Soil Science ◽

10.4141/cjss80-027 ◽

1980 ◽

Vol 60 (2) ◽

pp. 241-250 ◽

Cited By ~ 103

Author(s):

P. C. PANG ◽

E. A. PAUL

Keyword(s):

Dry Matter ◽

Nitrogen Transfer ◽

Apparent Difference ◽

Plant Materials ◽

Carbon And Nitrogen ◽

Vesicular Arbuscular ◽

Normal Atmospheric Pressure ◽

Mycorrhizal Plants ◽

The Difference ◽

Microbial Systems

A two-compartment growth chamber in which the aboveground plant materials were exposed to 14CO2 and the belowground portion was exposed to 15N2 under normal atmospheric pressure was designed for carbon and nitrogen transfer studies. Vicia faba infected with vesicular-arbuscular fungus Glomus mossae and non-mycorrhizal plants fixed similar quantities of N2 at an age of 6½ wk. Approximately 0.10 mg N was fixed∙g−1 dry plant materials∙day−1 and 40 mg C∙g−1 dry matter day−1 were synthesized by mycorrhizal and non-mycorrhizal fababeans during 48 h exposure to 14CO2 at 6½ wk with no apparent difference in yield of dry matter. The non-mycorrhizal plants transferred 37% of the fixed 14C beneath ground. The mycorrhizal ones transferred 47% of the fixed 14C beneath ground. Most of the difference could be accounted for in the belowground respiration. The 14CO2 produced by root-microbial systems of the mycorrhizal fababeans was twice as great as that of the nonmycorrhizal; both contained active rhizobium.

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