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

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.     

Interactions between arbuscular mycorrhizal fungi and soil bacteria

The soil environment is interesting and complicated. There are so many interactions taking place in the soil, which determine the properties of soil as a medium for the growth and activities of plants and soil microorganisms. The soil fungi, arbuscular mycorrhiza (AM), are in mutual and beneficial symbiosis with most of the terrestrial plants. AM fungi are continuously interactive with a wide range of soil microorganisms including nonbacterial soil microorganisms, plant growth promoting rhizobacteria, mycorrhiza helper bacteria and deleterious bacteria. Their interactions can have important implications in agriculture. There are some interesting interactions between the AM fungi and soil bacteria including the binding of soil bacteria to the fungal spore, the injection of molecules by bacteria into the fungal spore, the production of volatiles by bacteria and the degradation of fungal cellular wall. Such mechanisms can affect the expression of genes in AM fungi and hence their performance and ecosystem productivity. Hence, consideration of such interactive behavior is of significance. In this review, some of the most important findings regarding the interactions between AM fungi and soil bacteria with some new insights for future research are presented.     

Antagonism between bacteria and fungi: substrate competition and a possible tradeoff between fungal growth and tolerance towards bacteria

Bacteria and fungi often share a common substrate, and their spatial proximity in many environments has lead to either synergistic or antagonistic interactions. In this paper, the interaction of bacterial and fungal decomposers from an aquatic environment was studied. We found indications of a tradeoff between fungal growth and tolerance towards bacteria. Fungal strains growing best in absence of bacteria were most severely affected by bacterial presence, while those less suppressed during co-existence with bacteria had lower maximal growth rates in bacterial absence. Additionally, we show that the antagonism between bacteria and fungi is connected to competition for substrate, but that this competition can be drastically altered if fungi are given an opportunity to establish before inoculation of bacteria. Established fungi out-competed bacteria, and gained higher biomass than in simultaneously inoculated treatments with higher substrate concentrations.     

Volatile-mediated antagonism of soil bacterial communities against fungi

Competition is a major type of interaction between fungi and bacteria in soil and is also an important factor in suppression of plant diseases caused by soil-borne fungal pathogens. There is increasing attention for the possible role of volatiles in competitive interactions between bacteria and fungi. However, knowledge on the actual role of bacterial volatiles in interactions with fungi within soil microbial communities is lacking. Here, we examined colonization of sterile agricultural soils by fungi and bacteria from non-sterile soil inoculums during exposure to volatiles emitted by soil-derived bacterial communities. We found that colonization of soil by fungi was negatively affected by exposure to volatiles emitted by bacterial communities whereas that of bacteria was barely changed. Furthermore, there were strong effects of bacterial community volatiles on the assembly of fungal soil colonizers. Identification of volatile composition produced by bacterial communities revealed several compounds with known fungistatic activity. Our results are the first to reveal a collective volatile-mediated antagonism of soil bacteria against fungi. Given the better exploration abilities of filamentous fungi in unsaturated soils, this may be an important strategy for bacteria to defend occupied nutrient patches against invading fungi. Another implication of our research is that bacterial volatiles in soil atmospheres can have a major contribution to soil fungistasis.     

Differential expression of β-glucosidase in tomato — stress stimuli systems

In the present work the responses of β-glucosidase in leaves of tomato plants subjected to various stress factors of both pathogenic (fungi, bacteria, viruses) and abiotic origin (heat shock) were studied. Biochemical and cytochemical methods were applied. It was established that an increase of β-glucosidase activity is induced uniquely by fungal pathogens. The cytochemical tests confirm the finding. Hence, the conclusion can be drawn that β-glucosidase response is a specific character of fungal pathogenesis in tomato; probably, the enzyme is involved in plant — fungi recognition. The data are in accordance with our previous results on tobacco and wheat — stress stimuli systems.     

Antagonism between Bacteria and Fungi on Decomposing Aquatic Plant Litter

Bacterial and fungal decomposers of aquatic plant litter may exhibit either synergistic or antagonistic interactions, which are likely to influence microbial growth as well as the decomposition of litter and, eventually, the carbon metabolism of aquatic systems. To elucidate such interactions, we inoculated decomposing Phragmites culms in microcosms with fungal isolates and with natural communities of bacteria and fungi in different combinations. The development of fungal and bacterial biomass and the carbon dynamics were studied during several months of degradation. The results show a bilateral antagonistic relationship between bacteria and fungi. After 3 months, fungal biomass accumulation was approximately 12 times higher in the absence than in the presence of bacteria. Bacterial biomass accumulation was about double in the absence of fungi compared to when fungi were present. Similar interactions developed between a natural assemblage of bacteria and five different fungal strains isolated from Phragmites litter (three identified hyphomycetes and two unidentified strains). Despite the great difference in biomass development between the treatments, the carbon metabolism was similar regardless of whether fungi and/or bacteria were present alone or in coexistence. We suggest that the antagonism between bacteria and fungi is an important controlling factor for microbial colonization and growth on aquatic plant litter.     

A functional screen identifies lateral transfer of beta-glucuronidase (gus) from bacteria to fungi

Lateral gene transfer (LGT) from prokaryotes to microbial eukaryotes is usually detected by chance through genome-sequencing projects. Here, we explore a different, hypothesis-driven approach. We show that the fitness advantage associated with the transferred gene, typically invoked only in retrospect, can be used to design a functional screen capable of identifying postulated LGT cases. We hypothesized that beta-glucuronidase (gus) genes may be prone to LGT from bacteria to fungi (thought to lack gus) because this would enable fungi to utilize glucuronides in vertebrate urine as a carbon source. Using an enrichment procedure based on a glucose-releasing glucuronide analog (cellobiouronic acid), we isolated two gus(+) ascomycete fungi from soils (Penicillium canescens and Scopulariopsis sp.). A phylogenetic analysis suggested that their gus genes, as well as the gus genes identified in genomic sequences of the ascomycetes Aspergillus nidulans and Gibberella zeae, had been introgressed laterally from high-GC gram(+) bacteria. Two such bacteria (Arthrobacter spp.), isolated together with the gus(+) fungi, appeared to be the descendants of a bacterial donor organism from which gus had been transferred to fungi. This scenario was independently supported by similar substrate affinities of the encoded beta-glucuronidases, the absence of introns from fungal gus genes, and the similarity between the signal peptide-encoding 5' extensions of some fungal gus genes and the Arthrobacter sequences upstream of gus. Differences in the sequences of the fungal 5' extensions suggested at least two separate introgression events after the divergence of the two main Euascomycete classes. We suggest that deposition of glucuronides on soils as a result of the colonization of land by vertebrates may have favored LGT of gus from bacteria to fungi in soils.     

Host-induced gene silencing: a tool for understanding fungal host interaction and for developing novel disease control strategies

Recent discoveries regarding small RNAs and the mechanisms of gene silencing are providing new opportunities to explore fungal pathogen-host interactions and potential strategies for novel disease control. Plant pathogenic fungi are a constant and major threat to global food security; they represent the largest group of disease-causing agents on crop plants on the planet. An initial understanding of RNA silencing mechanisms and small RNAs was derived from model fungi. Now, new knowledge with practical implications for RNA silencing is beginning to emerge from the study of plant-fungus interactions. Recent studies have shown that the expression of silencing constructs in plants designed on fungal genes can specifically silence their targets in invading pathogenic fungi, such as Fusarium verticillioides, Blumeria graminis and Puccinia striiformis f.sp. tritici. Here, we highlight the important general aspects of RNA silencing mechanisms and emphasize recent findings from plant pathogenic fungi. Strategies to employ RNA silencing to investigate the basis of fungal pathogenesis are discussed. Finally, we address important aspects for the development of fungal-derived resistance through the expression of silencing constructs in host plants as a powerful strategy to control fungal disease.     

肠道真菌研究进展

摘要：肠道真菌是肠道微生物的重要组成部分，在肠道正常菌群中所占比例极小，主要包括假丝酵母属（Candida）、隐球酵母属（Cryptococcus）、青霉属（Penicillium）、曲霉属（Aspergillus）、红酵母属（Rhodotorula）等，对维持肠道微生态稳态和机体健康具有重要作用，也与抗生素相关性腹泻（AAD）、乙型肝炎、炎症性肠病（IBD）等疾病的发病机制息息相关。本文主要总结了目前已发现的肠道真菌属及其对人体的影响机制以及肠道真菌相关的研究方法，为肠道真菌在疾病的诊断和治疗方面的进一步研究提供依据与思路。     

Impact of white-rot fungi on numbers and community composition of bacteria colonizing beech wood from forest soil

White-rot fungi are important wood-decomposing organisms in forest ecosystems. Their ability to colonize and decompose woody resources may be strongly influenced by wood-inhabiting bacteria that grow on easily utilizable compounds e.g. oligomers of wood-polymers released by fungal enzymes. However, so far, it is not known how white-rot fungi deal with the presence of potential competing bacteria. Here, the effects of two white-rot fungi, Hypholoma fasciculare and Resinicium bicolor, on the numbers and composition of bacteria colonizing sterile beech wood blocks from forest soil are reported. Both total numbers (microscopic counts) and the numbers of cultivable wood-inhabiting bacteria were considerably lower in wood blocks that became colonized by the white-rot fungi than in control blocks. This points to the fungi out-competing the opportunistic bacteria. The presence of white-rot fungi resulted in a change in the relative abundance of families of cultivable bacteria in wood and also in a change of denaturing gradient gel electrophoresis patterns of directly amplified 16S rRNA gene fragments. Analysis of the bacterial community structure in soil adhering to exploratory mycelium (cords) indicated that fungal species-specific effects on bacterial community composition were also apparent in this fungal growth phase.     

Hypoxia and Fungal Pathogenesis: To Air or Not To Air?

Over the last 3 decades, the frequency of life-threatening human fungal infections has increased as advances in medical therapies, solid-organ and hematopoietic stem cell transplantations, an increasing geriatric population, and HIV infections have resulted in significant rises in susceptible patient populations. Although significant advances have been made in understanding how fungi cause disease, the dynamic microenvironments encountered by fungi during infection and the mechanisms by which they adapt to these microenvironments are not fully understood. As inhibiting and preventing in vivo fungal growth are main goals of antifungal therapies, understanding in vivo fungal metabolism in these host microenvironments is critical for the improvement of existing therapies or the design of new approaches. In this minireview, we focus on the emerging appreciation that pathogenic fungi like Candida albicans, Cryptococcus neoformans, and Aspergillus fumigatus are exposed to oxygen-limited or hypoxic microenvironments during fungal pathogenesis. The implications of these in vivo hypoxic microenvironments for fungal metabolism and pathogenesis are discussed with an aim toward understanding the potential impact of hypoxia on invasive fungal infection outcomes.     

A centralized resource for bacterial–fungal interactions research

Research on bacterial-fungal interactions (BFIs) has revealed that fungi and bacteria frequently interact with one another within diverse ecosystems and microbiomes. Assessing the current state of knowledge within the field of BFI research, particularly with respect to what interactions between bacteria and fungi have been previously described, is very challenging and time consuming. This is largely due to a lack of any centralized resource, with reports of BFIs being spread across publications in numerous journals using non-standardized text to describe the relationships. To address this issue, we have developed the BFI Research Portal, a publicly accessible database of previously reported interactions between bacterial and fungal taxa to serve as a centralized resource for the field. Users can query bacterial or fungal taxa to see what members from the other kingdom have been observed as interaction partners. Search results are accompanied by interactive and intuitive visual outputs, and the database is a dynamic resource that will be updated as new BFIs are reported.     

Wood decay fungi and their bacterial interaction partners in the built environment – A systematic review on fungal bacteria interactions in dead wood and timber

Microbial biodeterioration of timber and woody material in buildings can cause costly restoration procedures. Here, we focus on Serpula lacrymans (commonly known as dry-rot) the fungus causing the most severe damages to buildings in Europe. Although its morphology, lifestyle, and dispersal have been intensively studied, research on microorganisms sharing the same habitat and interacting with the dry-rot fungus is not as comprehensive. Bacteria have long been known to inhabit dead wood, and several studies have shown their association to fungi. However, their identity, ecology, and putative interactions with co-existing fungi in dead wood remains largely underexplored. The interactions of bacterial and fungi have considerable impact on all partners involved covering the full spectrum between antagonistic and beneficial. Fungi are highly capable of manipulating the microbial community in their surroundings (e.g. via pH manipulation) and bacteria, in turn, can influence fungi by affecting the outcomes of (antagonistic) interactions or preventing fungal feedback inhibition via consumption of breakdown products. Associated bacteria on the other side could play an essential role for the fungus as bacteria can exert significant influence on fungal physiology and behaviour. This minireview summarizes the current knowledge on bacterial-fungal interactions in dead wood with a special focus on dry-rot and proposes possible bacterial-fungal interaction (BFI) mechanisms based on examples from soil or decomposing wood from forests.     

Insights into the Phylogeny or Arylamine N-Acetyltransferases in Fungi

Previous studies have shown that Eumycetes fungi can acylate arylamine thanks to arylamine N-acetyltransferases, xenobiotic-metabolizing enzymes also found in animals and bacteria. In this article, we present the results of mining 96 available fungal genome sequences for arylamine N-acetyltransferase genes and propose their phylogeny. The filamentous Pezizomycotina are shown to possess many putative N-acetyltransferases, whilst these are often lacking in other fungal groups. The evolution of the N-acetyltransferases is best explained by the presence of at least one gene in the opisthokont ancestor of the fungi and animal kingdoms, followed by recurrent gene losses and gene duplications. A possible horizontal gene transfer event may have occurred from bacteria to the basidiomycetous yeast Malassezia globosa.     

Oxylipins and oxylipin synthesis pathways in fungi

Oxylipins are a family of oxygenated fatty acids that are very diverse with regard to origin, structure, and functions. These compounds are found in almost all living beings and serve both as autoregulators of the development of organisms and as communication molecules. The autoregulatory role of oxylipins in fungi is to control the development, reproduction, synthesis of secondary metabolites (including mycotoxins), and adaptive responses. The role of oxylipins in the regulation of pathogenesis accounts for an important aspect of research on the biological activity of these compounds. The synthetic pathways and functions of oxylipins of fungi, the differences between fungal oxylipins and oxylipins from bacteria, higher plants, and mammals, and the role of oxylipins in the interaction of fungi with other organisms are considered in the present review.     

内蒙草原不同植物功能群及物种对土壤微生物组成的影响

为了分析不同植物群落组成对内蒙古典型草原土壤微生物群落组成的影响,本研究利用植物功能群剔除处理实验平台,采用荧光定量PCR(real-timePCR)和自动核糖体间隔区基因分析(automated ribosomal intergenic spacer analysis,ARISA)技术,对不同植物功能群组成的非根际土壤和常见物种的根际土壤中细菌和真菌的数量及群落结构进行了分析。结果表明,在非根际土壤中,不同植物功能群组成对细菌数量有显著影响,而对真菌数量及细菌和真菌的群落结构影响不明显;在根际土壤中,不同植物物种对细菌、真菌的数量都有显著影响。此外,聚类分析表明,不同物种的根际土中细菌和真菌的群落结构也有所不同,尤其以细菌的群落结构变化较为明显。研究结果表明不同植物物种可以通过根系影响土壤微生物群落组成。     

Evolution of beta-lactam biosynthesis genes and recruitment of trans-acting factors

Penicillins and cephalosporins belong chemically to the group of beta-lactam antibiotics. The formation of hydrophobic penicillins has been reported in fungi only, notably Penicillium chrysogenum and Emericella nidulans, whereas the hydrophilic cephalosporins are produced by both fungi, e.g., Acremonium chrysogenum (cephalosporin C), and bacteria. The producing bacteria include Gram-negatives and Gram-positives, e.g. Lysobacter lactamdurans (cephabacins) and Streptomyces clavuligerus (cephamycin C), respectively. For a long time the evolutionary origin of beta-lactam biosynthesis genes in fungi has been discussed. As often, there are arguments for both hypotheses, i.e., horizontal gene transfer from bacteria to fungi versus vertical descent. There were strong arguments in favour of horizontal gene transfer, e.g., fungal genes were clustered or some genes lack introns. The recent identification and characterisation of cis-/trans-elements involved in the regulation of the beta-lactam biosynthesis genes has provided new arguments in favour of horizontal gene transfer. In contrast to the bacterium S. clavuligerus, all regulators of fungal beta-lactam biosynthesis genes represent wide-domain regulators which were recruited to also regulate the beta-lactam biosynthesis genes. Moreover, the fungal regulatory genes are not part of the gene cluster. If bacterial regulators were co-transferred with the gene cluster from bacteria to fungi, most likely they would have been non-functional in eukaryotes and lost during evolution. Alternatively, it is conceivable that only a part of the beta-lactam biosynthesis gene cluster was transferred to some fungi, e.g., the acvA and ipnA gene without a regulatory gene.     

Fungal infection in the oncologic clinic]

Fungal infection in oncologic hospitals is a serious threat for the patients that can undermine the results of the specific treatment of the main disease. Most frequently fungal infection is developing in localities naturally disseminated with microbial flora. The infection is usually mixed: bacterial/fungal and even fungal/fungal. The most frequent members of the associations are the representatives of Candida albicans: 63 per cent in the bacteria + fungi associations and up to 60 per cent in the fungi + fungi associations. The preventive use of azoles can lower the threat of fungal affection of the organs. However, the danger of mixed fungal/bacterial infection remains rather high.     

Diversity and biotechnological potential of the sponge-associated microbial consortia

Sponges are well known to harbor diverse microbes and represent a significant source of bioactive natural compounds derived from the marine environment. Recent studies of the microbial communities of marine sponges have uncovered previously undescribed species and an array of new chemical compounds. In contrast to natural compounds, studies on enzymes with biotechnological potential from microbes associated with sponges are rare although enzymes with novel activities that have potential medical and biotechnological applications have been identified from sponges and microbes associated with sponges. Both bacteria and fungi have been isolated from a wide range of marine sponge, but the diversity and symbiotic relationship of bacteria has been studied to a greater extent than that of fungi isolated from sponges. Molecular methods (e.g., rDNA, DGGE, and FISH) have revealed a great diversity of the unculturable bacteria and archaea. Metagenomic approaches have identified interesting metabolic pathways responsible for the production of natural compounds and may provide a new avenue to explore the microbial diversity and biotechnological potential of marine sponges. In addition, other eukaryotic organisms such as diatoms and unicellular algae from marine sponges are also being described using these molecular techniques. Many natural compounds derived from sponges are suspected to be of bacterial origin, but only a few studies have provided convincing evidence for symbiotic producers in sponges. Microbes in sponges exist in different associations with sponges including the true symbiosis. Fungi derived from marine sponges represent the single most prolific source of diverse bioactive marine fungal compounds found to date. There is a developing interest in determining the true diversity of fungi present in marine sponges and the nature of the association. Molecular methods will allow scientists to more accurately identify fungal species and determine actual diversity of sponge-associated fungi. This is especially important as greater cooperation between bacteriologists, mycologists, natural product chemists, and bioengineers is needed to provide a well-coordinated effort in studying the diversity, ecology, physiology, and association between bacteria, fungi, and other organisms present in marine sponges.     

Biohydrogenation of linoleic acid by rumen fungi compared with rumen bacteria

AIMS: To investigate biohydrogenation of linoleic acid by rumen fungi compared with rumen bacteria, and to identify the fungus with the fastest biohydrogenation rate. METHODS AND RESULTS: Biohydrogenation of linoleic acid by mixed rumen fungi and mixed rumen bacteria were compared in vitro. With mixed rumen bacteria, all biohydrogenation reactions were finished within 100 min of incubation and the end product of biohydrogenation was stearic acid. With mixed rumen fungi, biohydrogenation proceeded more slowly over a 24-h period. Conjugated linoleic acid (CLA; cis-9, trans-11 C18 : 2) was an intermediate product, and vaccenic acid (VA; trans-11 C18 : 1) was the end product of biohydrogenation. Fourteen pure fungal isolates were tested for biohydrogenation rate. DNA sequencing showed that the isolate with the fastest rate belonged to the Orpinomyces genus. CONCLUSIONS: It is concluded that rumen fungi have the ability to biohydrogenate linoleic acid, but biohydrogenation is slower in rumen fungi than in rumen bacteria. The end product of fungal biohydrogenation is VA, as for group A rumen bacteria. Orpinomyces is the most active biohydrogenating fungus. SIGNIFICANCE AND IMPACT OF THE STUDY: This is the first study to demonstrate that rumen fungi can biohydrogenate fatty acids. Fungi could influence CLA content of ruminant products.