Keystone Taxon Research Articles

Impact of a resistance gene against a fungal pathogen on the plant host residue microbiome: The case of the Leptosphaeria maculans–Brassica napus pathosystem

Oilseed rape residues are a crucial determinant of stem canker epidemiology as they support the sexual reproduction of the fungal pathogen Leptosphaeria maculans. The aim of this study was to characterize the impact of a resistance gene against L. maculans infection on residue microbial communities and to identify microorganisms interacting with this pathogen during residue degradation. We used near‐isogenic lines to obtain healthy and infected host plants. The microbiome associated with the two types of plant residues was characterized by metabarcoding. A combination of linear discriminant analysis and ecological network analysis was used to compare the microbial communities and to identify microorganisms interacting with L. maculans. Fungal community structure differed between the two lines at harvest, but not subsequently, suggesting that the presence/absence of the resistance gene influences the microbiome at the base of the stem whilst the plant is alive, but that this does not necessarily lead to differential colonization of the residues by fungi. Direct interactions with other members of the community involved many fungal and bacterial amplicon sequence variants (ASVs). L. maculans appeared to play a minor role in networks, whereas one ASV affiliated to Plenodomus biglobosus (synonym Leptosphaeria biglobosa) from the Leptosphaeria species complex may be considered a keystone taxon in the networks at harvest. This approach could be used to identify and promote microorganisms with beneficial effects against residue‐borne pathogens and, more broadly, to decipher the complex interactions between multispecies pathosystems and other microbial components in crop residues.

Disentangling the seasonal co-occurrence patterns and ecological stochasticity of planktonic and benthic bacterial communities within multiple lakes

Both the planktonic bacterial community (PBC) and benthic bacterial community (BBC) are important for biogeochemical processes in freshwater lakes. Despite their ecological significance, little is known about their seasonal co-occurrence patterns and the ecological processes that drive them. In this study, we aimed to investigate the ecological associations among bacterial taxa and assembly processes of PBC and BBC in different seasons. We used 16S rRNA gene high-throughput sequencing of a total of 150 water and sediment samples collected from multiple lakes distributed in an urban region of China during winter and summer. Our results revealed that PBC showed stronger seasonal variations in co-occurrence patterns than BBC, suggesting that BBC had greater temporal stability than PBC. Winter PBC network was characterized by higher connectivity and complexity, and thereby the formation of a highly stable community structure; whereas lower connectivity arising from the presence of fewer predicted keystone taxa (hubs and connectors in a network) was destabilizing to summer PBC network. In addition, the phylum Firmicutes identified as a putative keystone taxon of PBC in both seasons played a non-negligible role in maintaining network structure which may result from strong functional associations with other bacterioplankton. Temperature and pH were the best explanatory factors predicting the seasonal co-occurrence patterns of PBC and BBC, respectively. Normalized stochasticity ratio based on null-model analysis indicated that deterministic processes overwhelmed stochastic processes in governing the assembly of PBC and BBC in both seasons. However, we observed a greater influence of ecological stochasticity on BBC assembly than PBC assembly in both seasons. Taken together, these findings provide insights into understanding the impacts of habitat heterogeneity and seasonal variability on microbial assemblage patterns in lake ecosystems.

Proteomic Reference Map and Comparative Analysis between Streptomyces griseus S4-7 and wbiE2 Transcription Factor-Mutant Strain.

Streptomyces griseus S4-7, a well-characterized keystone taxon among strawberry microbial communities, shows exceptional disease-preventing ability. The whole-genome sequence, functional genes, and bioactive secondary metabolites of the strain have been described in previous studies. However, proteomics studies of not only the S4-7 strain, but also the Streptomyces genus as a whole, remain limited to date. Therefore, in the present study, we created a proteomics reference map for S. griseus S4-7. Additionally, analysis of differentially expressed proteins was performed against a wblE2 mutant, which was deficient in spore chain development and did not express an antifungal activity-regulatory transcription factor. We believe that our data provide a foundation for further in-depth studies of functional keystone taxa of the phytobiome and elucidation of the mechanisms underlying plant-microbe interactions, es-pecially those involving the Streptomyces genus.

Differential dynamics of microbial community networks help identify microorganisms interacting with residue-borne pathogens: the case of Zymoseptoria tritici in wheat

BackgroundWheat residues are a crucial determinant of the epidemiology of Septoria tritici blotch, as they support the sexual reproduction of the causal agent Zymoseptoria tritici. We aimed to characterize the effect of infection with this fungal pathogen on the microbial communities present on wheat residues and to identify microorganisms interacting with it. We used metabarcoding to characterize the microbiome associated with wheat residues placed outdoors, with and without preliminary Z. tritici inoculation, comparing the first set of residues in contact with the soil and a second set without contact with the soil, on four sampling dates in two consecutive years.ResultsThe diversity of the tested conditions, leading to the establishment of different microbial communities according to the origins of the constitutive taxa (plant only, or plant and soil), highlighted the effect of Z. tritici on the wheat residue microbiome. Several microorganisms were affected by Z. tritici infection, even after the disappearance of the pathogen. Linear discriminant analyses and ecological network analyses were combined to describe the communities affected by the infection. The number of fungi and bacteria promoted or inhibited by inoculation with Z. tritici decreased over time and was smaller for residues in contact with the soil. The interactions between the pathogen and other microorganisms appeared to be mostly indirect, despite the strong position of the pathogen as a keystone taxon in networks. Direct interactions with other members of the communities mostly involved fungi, including other wheat pathogens. Our results provide essential information about the alterations to the microbial community in wheat residues induced by the mere presence of a fungal pathogen, and vice versa. Species already described as beneficial or biocontrol agents were found to be affected by pathogen inoculation.ConclusionsThe strategy developed here can be viewed as a proof-of-concept focusing on crop residues as a particularly rich ecological compartment, with a high diversity of fungal and bacterial taxa originating from both the plant and soil compartments, and for Z. tritici-wheat as a model pathosystem. By revealing putative antagonistic interactions, this study paves the way for improving the biological control of residue-borne diseases.

Comparative genomics reveals complex natural product biosynthesis capacities and carbon metabolism across host-associated and free-living Aquimarina (Bacteroidetes, Flavobacteriaceae) species.

This study determines the natural product biosynthesis and full coding potential within the bacterial genus Aquimarina. Using comprehensive phylogenomics and functional genomics, we reveal that phylogeny instead of isolation source [host-associated (HA) vs. free-living (FL) habitats] primarily shape the inferred metabolism of Aquimarina species. These can be coherently organized into three major functional clusters, each presenting distinct natural product biosynthesis profiles suggesting that evolutionary trajectories strongly underpin their secondary metabolite repertoire and presumed bioactivities. Aquimarina spp. are highly versatile bacteria equipped to colonize HA and FL microniches, eventually displaying opportunistic behaviour, owing to their shared ability to produce multiple glycoside hydrolases from diverse families. We furthermore uncover previously underestimated, and highly complex secondary metabolism for the genus by detecting 928 biosynthetic gene clusters (BGCs) across all genomes, grouped in 439 BGC families, with polyketide synthases (PKSs), terpene synthases and non-ribosomal peptide synthetases (NRPSs) ranking as the most frequent BGCs encoding drug-like candidates. We demonstrate that the recently described cuniculene (trans-AT PKS) BGC is conserved among, and specific to, the here delineated A. megaterium-macrocephali-atlantica phylogenomic clade. Our findings provide a timely and in-depth perspective of an under-explored yet emerging keystone taxon in the cycling of organic matter and secondary metabolite production in marine ecosystems.

Long-term manure application increases soil organic matter and aggregation, and alters microbial community structure and keystone taxa

Microbes play pivotal roles in soil organic matter (SOM) turnover: formation and decomposition. Organic fertilizers play crucial role for SOM accumulation, aggregate formation and influence microbial community composition and co-occurrence networks in microhabitats. Here, we investigated prokaryotic and fungal communities and their co-occurrence networks in four aggregate size classes in upland Ultisol following 27 years of mineral and/or organic fertilizer (rice straw, peanut straw, radish, or pig manure) application. Organic fertilizers and aggregate size classes have main and interactive effects on SOM content in aggregates (p < 0.001). Aggregate size classes accounted for most of the variance (43%) of SOM content, with more SOM accumulated in macroaggregates (>250 μm) than microaggregates (<250 μm). Increased aggregate size affected prokaryotic and fungal community structure by increasing Rhizobiales and decreasing Eurotiales. Solibacterales and Mortierellales were particularly abundant in small microaggregates (<53 μm) due to substrate preferences. Organic fertilizers regulate microbial community structure more than aggregate size, accounting for 41% and 29% of variance in prokaryotic and fungal communities, respectively. Pig manure exerted the strongest effect on SOM content and aggregation, and influenced microbial community structure more strongly than plant residues, primarily by increasing Bacillales, Gaiellales and Pezizales, and decreasing Thermogemmatisporales. This effect of pig manure was related with efficient increase of SOM content and pH. Co-occurrence network analysis revealed more positive or negative linear relationships among microbial groups in microaggregates than in macroaggregates, indicating stronger synergistic and antagonistic microbial interactions in microaggregates with fewer favorable niches (higher recalcitrant SOM and less labile SOM). Thermogemmatisporales was identified as the most influential keystone taxon (relative abundance ∼4.9%) in soil, and its abundance rapidly diminished with increasing SOM content in macro- and microaggregates. Thus, microbial community structure is dependent on aggregate size, and this should be considered during sampling. Overall, long-term pig manure amendment increased the SOM content and aggregation, altering prokaryotic and fungal community structure and keystone taxa.

Effect of forest management on temperate ant communities

AbstractHuman management of ecosystems can have direct or indirect effects on species communities. How species communities are affected by management is a key question in ecology and nature conservation. As keystone taxon, changes in ant communities can have sustained consequences for entire ecosystems. In forests, management has been shown to have an overall negative effect on ant communities in tropical and a positive effect in boreal forests. However, in temperate forests, it is unclear what components of forest management affect ant communities and how. This study explores the direct and indirect effects of forest management on the taxonomic and functional diversity of ant communities in 150 temperate forest stands in three regions in Germany. Using a multi‐model inference approach and structural equation models, we analyzed the effects of 18 variables, including variables of forest management, forest structure, arthropod diversity, and biomass, as well as abiotic factors, on ant species richness, abundance, and functional trait diversity (Rao's Q) based on morphological (FDM) and life‐history traits (FDLH). In total, we found 28 ant species occurring on 120 plots. Main direct effects of forest management on ant abundance and species richness were caused by tree species selection, measured as dominant tree species. The main positive indirect effect was mediated by a reduced canopy cover with an increasing proportion of oak and pine, resulting in a higher temperature amplitude. Due to the low number of species in two regions, we analyzed functional diversity for the most ant species diverse region only. FDLH was affected positively by tree harvesting and negatively by structural complexity. FDM showed no response to forest management, potentially due to the low morphological diversity of temperate forest ants. Our results show that forest management practices in temperate forests strongly impact ant community structure. This can be beneficial for ants if management reduces the canopy cover, either by tree harvesting or by changing the tree species composition toward shade‐intolerant tree species. To promote ant diversity as key taxon for maintaining ecosystem processes in forest ecosystems, we suggest to integrate forest stands with more open and warmer conditions in future management strategies.

Diverse early dwarf mistletoes (Arceuthobium), ecological keystones of the Eocene Baltic amber biota.

Extant dwarf mistletoes (Arceuthobium M. Bieb., Viscaceae) are hemiparasites with complex roles in nature. They are one of the most severe pests in northern hemisphere conifer forests, but they also enhance the structural complexity and species diversity of the forests. Here, we describe the first pre-Miocene macrofossils of dwarf mistletoes. The fossils from Eocene Baltic amber provide new insights into the morphological evolution of the Arceuthobium lineage and its paleobiogeography. The amber inclusions were investigated with light microscopy and compared with extant Viscaceae and to historic descriptions of lost Baltic amber fossils with affinities to Viscaceae. Six fossil species of the Arceuthobium lineage, A. johnianum comb. nov., A. mengeanum comb. nov., A. conwentzii sp. nov., A. groehnii sp. nov., A. viscoides comb. nov. and A. obovatum sp. nov., occurred in source forests of Baltic amber, representing the oldest macrofossil evidence of dwarf mistletoes. They share morphological features of their bracts, internodes, fruits, and stomata with extant Arceuthobium. Differences from extant dwarf mistletoes, such as the perianth merosity, the nonfusion of squamate bracts and presence of oblanceolate expanded leaves, indicate their affiliation to an ancient lineage of the genus. The occurrence of six species of dwarf mistletoes in a single amber deposit suggests Arceuthobium was a keystone taxon of the Baltic amber source area. As in extant conifer forests, they probably influenced the structural complexity of the forest, not only leading to more open woodlands but also increasing species diversity, at least at a microhabitat scale.

Ecology of bacteria in the human gastrointestinal tract--identification of keystone and foundation taxa.

BackgroundDetermining ecological roles of community members and the impact of specific taxa on overall biodiversity in the gastrointestinal (GI) microbiota is of fundamental importance. A step towards a systems-level understanding of the GI microbiota is characterization of biotic interactions. Community time series analysis, an approach based on statistical analysis of changing population abundances within a single system over time, is needed in order to say with confidence that one population is affecting the dynamics of another.ResultsHere, we characterize biotic interaction structures and define ecological roles of major bacterial groups in four healthy individuals by analysing high-resolution, long-term (>180 days) GI bacterial community time series. Actinobacteria fit the description of a keystone taxon since they are relatively rare, but have a high degree of ecological connectedness, and are positively correlated with diversity both within and between individuals. Bacteriodetes were found to be a foundation taxon in that they are numerically dominant and interact extensively, in particular through positive interactions, with other taxa. Although community structure, diversity and biotic interaction patterns were specific to each individual, we observed a strong tendency towards more intense competition within than between phyla. This is in agreement with Darwin’s limiting similarity hypothesis as well as a published biotic interaction model of the GI microbiota based on reverse ecology. Finally, we link temporal enterotype switching to a reciprocal positive interaction between two key genera.ConclusionsIn this study, we identified ecological roles of key taxa in the human GI microbiota and compared our time series analysis results with those obtained through a reverse ecology approach, providing further evidence in favour of the limiting similarity hypothesis first put forth by Darwin. Larger longitudinal studies are warranted in order to evaluate the generality of basic ecological concepts as applied to the GI microbiota, but our results provide a starting point for achieving a more profound understanding of the GI microbiota as an ecological system.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-015-0107-4) contains supplementary material, which is available to authorized users.

Squamate phylogeny and the relationships of snakes and mosasauroids

Abstract Cladistic analysis of extant and fossil squamates (95 characters, 26 taxa) finds the fossil squamate,Coniasaurus Owen, 1850, to be the sister-group of the Mosasauroidea (mosasaurs and aigialosaurs). This clade is supported in all 18 shortest cladograms (464 steps; CI 0.677; HI 0.772) by nine characters of the dermatocranium, maxilla, and mandible. A Strict Consensus Tree of the 18 shortest trees collapses to a basal polytomy for most major squamate clades including the clade (Coniasaurus, Mosasauroidea). A Majority Rule Consensus Tree shows that, in 12 of 18 shortest cladograms, the cladeConiasaurus –Mosasauroidea is the sister-group to snakes (Scolecophidia (Alethinophidia, Dinilysia); this entire clade, referred to as the Pythonomorpha ([[Scolecophidia [Alethinophidia, Dinilysia]], [Coniasaurus, Mosasauroidea]]) is the sister-group to all other scleroglossans. Pythonomorpha is supported in these 12 cladograms by nine characters related to the lower jaw and cranial kinesis. In 6 of 18 shortest cladograms, snakes are the sister-group to the clade (Amphisbaenia (Dibamidae (Gekkonoidea, Eublepharidae))). None of the cladograms support the hypothesis that coniasaurs and mosasauroids are derived varanoid anguimorphs. Two additional analyses were conducted: (1) manipulation and movement of problematic squamate clades while constraining «accepted» relationships; (2) additional cladistic analyses beginning with extant taxa, and sequentially adding fossil taxa. From Test I, at 467 steps, Pythonomorpha can be the sister-group to the Anguimorpha, Scincomorpha, «scinco-gekkonomorpha» [scincomorphs, gekkotans, and amphibaenids-dibamids]. At 471 steps Pythonomorpha can be placed within Varanoidea. Treating only mosasauroids and coniasaurs as a monophyletic group: 469 steps, mosasauroids and coniasaurs as sister-group to Anguimorpha; 479 steps, mosasauroids and coniasaurs nested within Varanoidea. Test II finds snakes to nest within Anguimorpha in a data set of only Mosasauroidea+Extant Squamates; the sistergroup to snakes+anugimorphs is (Amphisbaenia (Dibamidae (Gekkonoidea, Eublepharidae))). No one particular taxon is identified as a keystone taxon in this analysis, though it appears true that fossil taxa significantly alter the structure of squamate phylogenetic trees.

Squamate phylogeny and the relationships of snakes and mosasauroids

Cladistic analysis of extant and fossil squamates (95 characters, 26 taxa) finds the fossil squamate,Coniasaurus Owen, 1850, to be the sister-group of the Mosasauroidea (mosasaurs and aigialosaurs). This clade is supported in all 18 shortest cladograms (464 steps; CI 0.677; HI 0.772) by nine characters of the dermatocranium, maxilla, and mandible. A Strict Consensus Tree of the 18 shortest trees collapses to a basal polytomy for most major squamate clades including the clade (Coniasaurus, Mosasauroidea). A Majority Rule Consensus Tree shows that, in 12 of 18 shortest cladograms, the cladeConiasaurus –Mosasauroidea is the sister-group to snakes (Scolecophidia (Alethinophidia, Dinilysia); this entire clade, referred to as the Pythonomorpha ([[Scolecophidia [Alethinophidia, Dinilysia]], [Coniasaurus, Mosasauroidea]]) is the sister-group to all other scleroglossans. Pythonomorpha is supported in these 12 cladograms by nine characters related to the lower jaw and cranial kinesis. In 6 of 18 shortest cladograms, snakes are the sister-group to the clade (Amphisbaenia (Dibamidae (Gekkonoidea, Eublepharidae))). None of the cladograms support the hypothesis that coniasaurs and mosasauroids are derived varanoid anguimorphs. Two additional analyses were conducted: (1) manipulation and movement of problematic squamate clades while constraining «accepted» relationships; (2) additional cladistic analyses beginning with extant taxa, and sequentially adding fossil taxa. From Test I, at 467 steps, Pythonomorpha can be the sister-group to the Anguimorpha, Scincomorpha, «scinco-gekkonomorpha» [scincomorphs, gekkotans, and amphibaenids-dibamids]. At 471 steps Pythonomorpha can be placed within Varanoidea. Treating only mosasauroids and coniasaurs as a monophyletic group: 469 steps, mosasauroids and coniasaurs as sister-group to Anguimorpha; 479 steps, mosasauroids and coniasaurs nested within Varanoidea. Test II finds snakes to nest within Anguimorpha in a data set of only Mosasauroidea+Extant Squamates; the sistergroup to snakes+anugimorphs is (Amphisbaenia (Dibamidae (Gekkonoidea, Eublepharidae))). No one particular taxon is identified as a keystone taxon in this analysis, though it appears true that fossil taxa significantly alter the structure of squamate phylogenetic trees.