Fritz Oehl

Impact of Land Use Intensity on the Species Diversity of Arbuscular Mycorrhizal Fungi in Agroecosystems of Central Europe

ABSTRACT The impact of land use intensity on the diversity of arbuscular mycorrhizal fungi (AMF) was investigated at eight sites in the “three-country corner” of France, Germany, and Switzerland. Three sites were low-input, species-rich grasslands. Two sites represented low- to moderate-input farming with a 7-year crop rotation, and three sites represented high-input continuous maize monocropping. Representative soil samples were taken, and the AMF spores present were morphologically identified and counted. The same soil samples also served as inocula for “AMF trap cultures” with Plantago lanceolata, Trifolium pratense, and Lolium perenne. These trap cultures were established in pots in a greenhouse, and AMF root colonization and spore formation were monitored over 8 months. For the field samples, the numbers of AMF spores and species were highest in the grasslands, lower in the low- and moderate-input arable lands, and lowest in the lands with intensive continuous maize monocropping. Some AMF species occurred at all sites (“generalists”); most of them were prevalent in the intensively managed arable lands. Many other species, particularly those forming sporocarps, appeared to be specialists for grasslands. Only a few species were specialized on the arable lands with crop rotation, and only one species was restricted to the high-input maize sites. In the trap culture experiment, the rate of root colonization by AMF was highest with inocula from the permanent grasslands and lowest with those from the high-input monocropping sites. In contrast, AMF spore formation was slowest with the former inocula and fastest with the latter inocula. In conclusion, the increased land use intensity was correlated with a decrease in AMF species richness and with a preferential selection of species that colonized roots slowly but formed spores rapidly.

Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity

Communities of arbuscular mycorrhizal fungi (AMF) in five agricultural field sites of different management intensities were studied. Variable regions of the ribosomal RNA genes were used to detect and identify AMF directly within colonized roots. Roots from a continuous maize monoculture showed low AMF diversity, in agreement with previous reports on molecular diversity of AMF in agricultural soils. In contrast, a substantially higher diversity of AMF was found throughout the long term ‘DOK’ field experiment, where organic and conventional agricultural practices have been compared side by side since 1978. In this experiment, a 7‐year crop rotation is performed under lower levels of inorganic fertilizer input and chemical pest control. These results are in good agreement with analyses of the spore community previously conducted in these field sites. In a third site, an organically managed leek field with soil of very high phosphate content reflecting the highly intensive conventional field history and intensive tillage, we detected a low‐diversity community comparable to the maize monoculture. In addition to fungi from Glomus group A, which have previously been reported to dominate arable soils, we regularly found members of the genera Scutellospora, Paraglomus and Acaulospora. The genus Acaulospora was shown to occur more frequently early in the growing season, suggesting that the life history strategy of AMF may influence the active community at a given time. These data show that the diversity of AMF is not always low in arable soils. Furthermore, low‐input agriculture involving crop rotation may provide better conditions to preserve AMF diversity, by preventing the selection for the few AMF taxa tolerating high nutrient levels.

Advances in Glomeromycota taxonomy and classification

Concomitant morphological and molecular analyses have led to major breakthroughs in the taxonomic organization of the phylum Glomeromycota. Fungi in this phylum are known to form arbuscular mycorrhiza, and so far three classes, five orders, 14 families and 29 genera have been described. Sensu lato, spore formation in 10 of the arbuscular mycorrhiza-forming genera is exclusively glomoid, one is gigasporoid, seven are scutellosporoid, four are entrophosporoid, two are acaulosporoid, and one is pacisporoid. Spore bimorphism is found in three genera, and one genus is associated with cyanobacteria. Here we present the current classification developed in several recent publications and provide a summary to facilitate the identification of taxa from genus to class level.

Rhizoglomus, a new genus of the Glomeraceae

Rhizoglomus gen. nov. (Glomeraceae, Glomeromycetes) is proposed, typified by Glomus intraradices [≡ Rhizoglomus intraradices]. The genus encompasses species of arbuscular mycorrhizal fungi that frequently form abundant spores in soil and roots and is morphologically characterized by spores with cylindrical subtending hyphae (usually with an open pore at the base) and at least two or three (rarely up to five) distinct wall layers. Phylogenetically, the genus forms a separate clade in the Glomeraceae. In addition to R. intraradices, the genus includes R. aggregatum, R. antarcticum, R. arabicum, R. clarum, R. custos, R. fasciculatum, R. invermaium, R. irregulare, R. manihotis, R. microaggregatum, R. natalense, and R. proliferum. Some of these species were previously assigned to Rhizophagus (type: R. populinus), a pathogenic genus that does not belong in the Glomeromycota.

Acaulospora alpina, a new arbuscular mycorrhizal fungal species characteristic for high mountainous and alpine regions of the Swiss Alps

Acaulospora alpina sp. nov. forms small (65–85 μm diam), dark yellow to orange-brown spores laterally on the neck of hyaline to subhyaline sporiferous saccules. The spores have a three-layered outer spore wall, a bi-layered middle wall and a three-layered inner wall. The surface of the second layer of the outer spore wall is ornamented, having regular, circular pits (1.5–2 μm diam) that are as deep as wide and truncated conical. A “beaded” wall layer as found in most other Acaulospora spp. is lacking. The spore morphology of A. alpina resembles that of A. paulinae but can be differentiated easily by the unique ornamentation with the characteristic pits and by the spore color. A key is presented summarizing the morphological differences among Acaulospora species with an ornamented outer spore wall. Partial DNA sequences of the ITS1, 5.8S subunit and ITS2 regions of ribosomal DNA show that A. alpina and A. paulinae are not closely related. Acaulospora lacunosa, which has similar color but has generally bigger spores, also has distinct rDNA sequences. Acaulospora alpina is a characteristic member of the arbuscular mycorrhizal fungal communities in soils with pH 3.5–6.5 in grasslands of the Swiss Alps at altitudes between 1800 and 2700 m above sea level. It is less frequent at 1300–1800 m above sea level, and it so far has not been found in the Alps below 1300 m or in the lowlands of Switzerland.

Agricultural practices indirectly influence plant productivity and ecosystem services through effects on soil biota

It is well established that agricultural practices alter the composition and diversity of soil microbial communities. However, the impact of changing soil microbial communities on the functioning of the agroecosystems is still poorly understood. Earlier work showed that soil tillage drastically altered microbial community composition. Here we tested, using an experimental grassland (Lolium, Trifolium, Plantago) as a model system, whether soil microbial communities from conventionally tilled (CT) and non-tilled (NT) soils have different influences on plant productivity and nutrient acquisition. We specifically focus on arbuscular mycorrhizal fungi (AMF), as they are a group of beneficial soil fungi that can promote plant productivity and ecosystem functioning and are also strongly affected by tillage management. Soil microbial communities from CT and NT soils varied greatly in their effects on the grassland communities. Communities from CT soil increased overall biomass production more than soil communities from NT soil. This effect was mainly due to a significant growth promotion of Trifolium by CT microorganisms. In contrast to CT soil inoculum, NT soil inoculum increased plant phosphorus concentration and total plant P content, demonstrating that the soil microbial communities from NT fields enhance P uptake. Differences in AM fungal community composition resulting, for instance, in twofold greater hyphal length in NT soil communities when compared to CT, are the most likely explanation for the different plant responses to CT and NT soil inocula. A range of field studies have shown that plant P uptake increases when farmers change to conservation tillage or direct seeding. Our results indicate that this enhanced P uptake results from enhanced hyphal length and an altered AM fungal community. Our results further demonstrate that agricultural management practices indirectly influence ecosystem services and plant community structure through effects on soil biota.

Otospora bareai, a new fungal species in the Glomeromycetes from a dolomitic shrub land in Sierra de Baza National Park (Granada, Spain)

A new fungal species of the Glomeromycetes was isolated from the rhizosphere of Pterocephalus spathulatus and Thymus granatensis, two rare endemic plants growing on dolomite in the Sierra de Baza (Granada, southern Spain). The fungus was propagated in pot cultures of Sorghum vulgare and Trifolium pratense for 4 y and it is described here on the basis of the spores found in nature and formed in pot cultures. Its brown spores (140–210 μm diam) form laterally on a persistent, brown stalk (=neck) of a sporiferous saccule. They have two walls without ornamentation: a brown, three- to four-layered outer wall and a hyaline two- to three-layered inner wall. The unique combination of spore formation and spore wall structure does not fit with any of the known fungal genera. Spore formation is similar to that of Acaulospora spp. and Archaeospora trappei, but Acaulospora spp. has three spore walls with a characteristic “beaded” wall, and the outer wall of Ar. trappei is simple, thin, hyaline and only bilayered. Spore wall structure of the new fungus is similar to that of Entrophospora infrequens, however this fungus forms its spores internally, inside the hyphal stalk of the sporiferous saccule. Molecular analyses of the small subunit of the ribosomal gene phylogenetically place the new fungus next to Diversispora spurca, which forms one-walled glomoid spores (i.e. terminally on hyphae). Based on these analyses we place the new fungus into a new genus in the family Diversisporaceae under the epithet Otospora bareai.

Intraornatosporaceae ( Gigasporales ), a new family with two new genera and two new species

A new family (Intraornatosporaceae), two new genera (Intraornatospora, Paradentiscutata), two new species (P. bahiana, P. maritima), and a new combination (I. intraornata) are presented in the Gigasporales. The genera, both with diagnostic introverted ornamentations on the spore wall, are distinguished by spore wall structure and germ shield characteristics. The new species, detected in NE Brazil, can be differentiated by their projections on the outer spore surface. Partial sequences of the LSU rRNA gene place both species next to I. intraornata in a monophyletic major clade related to Gigasporaceae and Dentiscutataceae.

A novel clade of sporocarp-forming species of glomeromycotan fungi in the Diversisporales lineage

In the early times of taxonomy of arbuscular mycorrhizal fungi (Glomeromycota), exclusively sporocarpic species were described. Since then the focus has mainly shifted to species forming spores singly. For many of the sporocarpic species, no molecular data have been made available, and their phylogenetic position has remained unclear. We obtained small subunit ribosomal rDNA and internal transcribed spacer data from specimens of glomeromycotan sporocarps from tropical areas that were assigned to three morphospecies. The complete sequence of the 18S small rDNA subunit sequence, internal transcribed spacers (ITS) 1 and 2 and 5.8S rDNA subunit, was determined from a sporocarp of Glomus fulvum. Partial sequences of the small subunit and the other regions were obtained from Glomus pulvinatum and the newly described species Glomus megalocarpum. Molecular phylogenetic analyses placed all species analyzed as a monophyletic sister group to the Diversispora spurca/Glomus versiforme clade group (“Glomus group C”) within the Diversisporales. The phylogenetic divergence from other known species suggests that this clade may constitute a new genus. These findings will have important consequences for taxon definition in the Diversisporales. They will facilitate identification of these fungi using rDNA sequences within colonized roots or the environment.

Unique arbuscular mycorrhizal fungal communities uncovered in date palm plantations and surrounding desert habitats of Southern Arabia

The main objective of this study was to shed light on the previously unknown arbuscular mycorrhizal fungal (AMF) communities in Southern Arabia. We explored AMF communities in two date palm (Phoenix dactylifera) plantations and the natural vegetation of their surrounding arid habitats. The plantations were managed traditionally in an oasis and according to conventional guidelines at an experimental station. Based on spore morphotyping, the AMF communities under the date palms appeared to be quite diverse at both plantations and more similar to each other than to the communities under the ruderal plant, Polygala erioptera, growing at the experimental station on the dry strip between the palm trees, and to the communities uncovered under the native vegetation (Zygophyllum hamiense, Salvadora persica, Prosopis cineraria, inter-plant area) of adjacent undisturbed arid habitat. AMF spore abundance and species richness were higher under date palms than under the ruderal and native plants. Sampling in a remote sand dune area under Heliotropium kotschyi yielded only two AMF morphospecies and only after trap culturing. Overall, 25 AMF morphospecies were detected encompassing all study habitats. Eighteen belonged to the genus Glomus including four undescribed species. Glomus sinuosum, a species typically found in undisturbed habitats, was the most frequently occurring morphospecies under the date palms. Using molecular tools, it was also found as a phylogenetic taxon associated with date palm roots. These roots were associated with nine phylogenetic taxa, among them eight from Glomus group A, but the majority could not be assigned to known morphospecies or to environmental sequences in public databases. Some phylogenetic taxa seemed to be site specific. Despite the use of group-specific primers and efficient trapping systems with a bait plant consortium, surprisingly, two of the globally most frequently found species, Glomus intraradices and Glomus mosseae, were not detected neither as phylogenetic taxa in the date palm roots nor as spores under the date palms, the intermediate ruderal plant, or the surrounding natural vegetation. The results highlight the uniqueness of AMF communities inhabiting these diverse habitats exposed to the harsh climatic conditions of Southern Arabia.