Species-specific Communities Research Articles

Bacterial diversity in arboreal ant nesting spaces is linked to colony developmental stage

The omnipresence of ants is commonly attributed to their eusocial organization and division of labor, however, bacteria in their nests may facilitate their success. Like many other arboreal ants living in plant-provided cavities, Azteca ants form dark-colored “patches” in their nesting space inside Cecropia host plants. These patches are inhabited by bacteria, fungi and nematodes and appear to be essential for ant colony development. Yet, detailed knowledge of the microbial community composition and its consistency throughout the life cycle of ant colonies was lacking. Amplicon sequencing of the microbial 16S rRNA genes in patches from established ant colonies reveals a highly diverse, ant species-specific bacterial community and little variation within an individual ant colony, with Burkholderiales, Rhizobiales and Chitinophagales being most abundant. In contrast, bacterial communities of early ant colony stages show low alpha diversity and no ant species-specific community composition. We suggest a substrate-caused bottleneck after vertical transmission of the bacterial patch community from mother to daughter colonies. The subsequent ecological succession is driven by environmental parameters and influenced by ant behavior. Our study provides key information for future investigations determining the functions of these bacteria, which is essential to understand the ubiquity of such patches among arboreal ants.

Taurine as a key intermediate for host-symbiont interaction in the tropical sponge Ianthella basta

Marine sponges are critical components of marine benthic fauna assemblages, where their filter-feeding and reef-building capabilities provide bentho-pelagic coupling and crucial habitat. As potentially the oldest representation of a metazoan-microbe symbiosis, they also harbor dense, diverse, and species-specific communities of microbes, which are increasingly recognized for their contributions to dissolved organic matter (DOM) processing. Recent omics-based studies of marine sponge microbiomes have proposed numerous pathways of dissolved metabolite exchange between the host and symbionts within the context of the surrounding environment, but few studies have sought to experimentally interrogate these pathways. By using a combination of metaproteogenomics and laboratory incubations coupled with isotope-based functional assays, we showed that the dominant gammaproteobacterial symbiont, ‘Candidatus Taurinisymbion ianthellae’, residing in the marine sponge, Ianthella basta, expresses a pathway for the import and dissimilation of taurine, a ubiquitously occurring sulfonate metabolite in marine sponges. ‘Candidatus Taurinisymbion ianthellae’ incorporates taurine-derived carbon and nitrogen while, at the same time, oxidizing the dissimilated sulfite into sulfate for export. Furthermore, we found that taurine-derived ammonia is exported by the symbiont for immediate oxidation by the dominant ammonia-oxidizing thaumarchaeal symbiont, ‘Candidatus Nitrosospongia ianthellae’. Metaproteogenomic analyses also suggest that ‘Candidatus Taurinisymbion ianthellae’ imports DMSP and possesses both pathways for DMSP demethylation and cleavage, enabling it to use this compound as a carbon and sulfur source for biomass, as well as for energy conservation. These results highlight the important role of biogenic sulfur compounds in the interplay between Ianthella basta and its microbial symbionts.

Influence of invasive earthworms (Amynthas spp.) on Wisconsin forest soil microbial communities and soil chemistry

The invasion of Amynthas species complex of earthworms from Asia into North American hardwood forests poses a novel threat to these ecosystems. These species can competitively exclude previously-established earthworms, have novel effects on microbial communities, and influence the structural and chemical composition of soils differently than other earthworm species. However, because prior research has found that earthworm species is an important factor for microbial community composition, Amynthas species may also uniquely affect soil microbial community composition. To address this, we took earthworm and soil samples from 0.5-m quadrats along an active invasion front of Amynthas agrestis and A. tokioensis at the University of Wisconsin-Madison Arboretum. We tested all soil samples for basal metabolic rates, total carbon, and total nitrogen. We also extracted microbial DNA from cast samples, dissected worm guts, and soil samples, and we used high-throughput DNA sequencing to characterize Amynthas species-specific differences in bacterial and fungal community composition. We found that plots that had been occupied by Amynthas for longer than a year had higher total nitrogen, lower C/N, and different communities of soil bacteria and fungi when compared to newly-invaded plots. We also found that Amynthas had species-specific differences in bacterial communities adhered to worm guts and in worm casts. These results suggest that Amynthas species introduce novel assemblages of bacteria and fungi through their casts, and these differences are associated with the species-specific community composition of earthworm guts. These results also suggest that Amynthas species are likely affecting the soil microbial community during invasion.

Characterization of a sponge microbiome using an integrative genome-centric approach.

Marine sponges often host diverse and species-specific communities of microorganisms that are critical for host health. Previous functional genomic investigations of the sponge microbiome have focused primarily on specific symbiont lineages, which frequently make up only a small fraction of the overall community. Here, we undertook genome-centric analysis of the symbiont community in the model species Ircinia ramosa and analyzed 259 unique, high-quality metagenome-assembled genomes (MAGs) that comprised 74% of the I. ramosa microbiome. Addition of these MAGs to genome trees containing all publicly available microbial sponge symbionts increased phylogenetic diversity by 32% within the archaea and 41% within the bacteria. Metabolic reconstruction of the MAGs showed extensive redundancy across taxa for pathways involved in carbon fixation, B-vitamin synthesis, taurine metabolism, sulfite oxidation, and most steps of nitrogen metabolism. Through the acquisition of all major taxa present within the I. ramosa microbiome, we were able to analyze the functional potential of a sponge-associated microbial community in unprecedented detail. Critical functions, such as carbon fixation, which had previously only been assigned to a restricted set of sponge-associated organisms, were actually spread across diverse symbiont taxa, whereas other essential pathways, such as ammonia oxidation, were confined to specific keystone taxa.

Local biotic interactions drive species-specific divergence in soil bacterial communities.

It is well accepted that environmental heterogeneity and dispersal are key factors determining soil bacterial community composition, yet little is known about the role of local biotic interactions. Here we address this issue with an abundance-manipulation experiment that was conducted in a semiarid grassland. We manually increased the abundance of six randomly chosen resident bacterial species in separate, closed, communities and allowed the communities to recover in situ for 1 year. The single episode of increase in the abundance of different species drove species-specific community divergence accompanied by a decline in local diversity. Four of the six added species caused a decrease in the abundance of their closely related species, suggesting an important role of interspecific competition in driving the observed community divergence. Our results also suggested a lack of effective population regulations to force the relative abundance of manipulated species to revert to original level, which would allow persistence of the divergence among soil bacterial communities. We concluded that biotic interactions were important in determining soil bacterial community composition, which could result in substantial variation in soil bacterial community composition in abiotically homogenous environment.

Associated bacteria of Botryococcus braunii (Chlorophyta).

Botryococcus braunii (Chlorophyta) is a green microalga known for producing hydrocarbons and exopolysaccharides (EPS). Improving the biomass productivity of B. braunii and hence, the productivity of the hydrocarbons and of the EPS, will make B. braunii more attractive for industries. Microalgae usually cohabit with bacteria which leads to the formation of species-specific communities with environmental and biological advantages. Bacteria have been found and identified with a few B. braunii strains, but little is known about the bacterial community across the different strains. A better knowledge of the bacterial community of B. braunii will help to optimize the biomass productivity, hydrocarbons, and EPS accumulation. To better understand the bacterial community diversity of B. braunii, we screened 12 strains from culture collections. Using 16S rRNA gene analysis by MiSeq we described the bacterial diversity across 12 B. braunii strains and identified possible shared communities. We found three bacterial families common to all strains: Rhizobiaceae, Bradyrhizobiaceae, and Comamonadaceae. Additionally, the results also suggest that each strain has its own specific bacteria that may be the result of long-term isolated culture.

Stoichiometry patterns of plant organ N and P in coastal herbaceous wetlands along the East China Sea: implications for biogeochemical niche

Nitrogen (N) and phosphorus (P) are essential nutrients for plant growth, and their availability and stoichiometry play pivotal roles in trophic dynamics and community composition. The biogeochemical niche (BN) hypothesis claims that each species should have an optimal elemental composition and stoichiometry as a consequence of its optimal function in its specific ecological niche. Little attention, however, has been given to N and P stoichiometric patterns and test the BN hypothesis in coastal wetland communities from the perspective of organ and species-specific comparisons. We investigated factors responsible for changes in N and P stoichiometry patterns in different functional groups in coastal wetlands and tested the BN hypothesis by evaluating N and P composition in whole aboveground plants and organs. Both plant N and P concentrations were high in coastal wetlands, indicating that N and P were not likely limiting, although the N:P ratio was slightly lower than the ratio reported in global and Chinese terrestrial flora. N and P concentrations and N:P ratios varied strongly between C3 and C4 species, among species, and among organs within species. N and P concentrations were not correlated with latitude, mean annual temperature and precipitation, although N:P ratio was weakly correlated with these factors. The differences in N and P concentrations and N:P ratios along the wetland gradients were mainly because of the species-specific community composition of each site. The results are consistent with the BN hypothesis. First, N and P composition is species-specific (homeostatic component of BN), each species tends to maintain its own composition even growing in different sites with different species composition. Second, different species, despite maintaining their own composition, have distinct degree of composition phenotypic flexibility (flexibility component of BN); this different size of “biogeochemical space” was observed when comparing different species living in the same community and the shifts in species BN space and size was observed when comparing populations of the same species living in different sites.

Seasonal variation of bacterial endophytes in urban trees.

Bacterial endophytes, non-pathogenic bacteria residing within plants, contribute to the growth and development of plants and their ability to adapt to adverse conditions. In order to fully exploit the capabilities of these bacteria, it is necessary to understand the extent to which endophytic communities vary between species and over time. The endophytes of Acer negundo, Ulmus pumila, and Ulmus parvifolia were sampled over three seasons and analyzed using culture dependent and independent methods (culture on two media, terminal restriction fragment length polymorphism, and tagged pyrosequencing of 16S ribosomal amplicons). The majority of culturable endophytes isolated were Actinobacteria, and all the samples harbored Bacillus, Curtobacterium, Frigoribacterium, Methylobacterium, Paenibacilllus, and Sphingomonas species. Regardless of culture medium used, only the culturable communities obtained in the winter for A. negundo could be distinguished from those of Ulmus spp. In contrast, the nonculturable communities were dominated by Proteobacteria and Actinobacteria, particularly Erwinia, Ralstonia, and Sanguibacter spp. The presence and abundance of various bacterial classes and phyla changed with the changing seasons. Multivariate analysis on the culture independent data revealed significant community differences between the endophytic communities of A. negundo and Ulmus spp., but overall season was the main determinant of endophytic community structure. This study suggests studies on endophytic populations of urban trees should expect to find significant seasonal and species-specific community differences and sampling should proceed accordingly.

Host-specific microbial communities in three sympatric North Sea sponges.

The establishment of next-generation technology sequencing has deepened our knowledge of marine sponge-associated microbiota with the identification of at least 32 phyla of Bacteria and Archaea from a large number of sponge species. In this study, we assessed the diversity of the microbial communities hosted by three sympatric sponges living in a semi-enclosed North Sea environment using pyrosequencing of bacterial and archaeal 16S ribosomal RNA gene fragments. The three sponges harbor species-specific communities each dominated by a different class of Proteobacteria. An α-proteobacterial Rhodobacter-like phylotype was confirmed as the predominant symbiont of Halichondria panicea. The microbial communities of Haliclona xena and H. oculata are described for the first time in this study and are dominated by Gammaproteobacteria and Betaproteobacteria, respectively. Several common phylotypes belonging to Chlamydiae, TM6, Actinobacteria, and Betaproteobacteria were detected in all sponge samples. A number of phylotypes of the phylum Chlamydiae were present at an unprecedentedly high relative abundance of up to 14.4 ± 1.4% of the total reads, which suggests an important ecological role in North Sea sponges. These Chlamydiae-affiliated operational taxonomic units may represent novel lineages at least at the genus level as they are only 86-92% similar to known sequences.

Deep sequencing reveals diversity and community structure of complex microbiota in five Mediterranean sponges

Marine sponges harbor dense microbial communities of exceptionally high diversity. Despite the complexity of sponge microbiota, microbial communities in different sponges seem to be remarkably similar. In this study, we used a subset of a previously established 454 amplicon pyrosequencing dataset (Schmitt and Taylor, unpublished data). Five Mediterranean sponges were chosen including the model sponge Aplysina aerophoba to determine the extent of uniformity by defining (i) the core microbial community, consisting of bacteria found in all sponges, (ii) the variable microbial community, consisting of bacteria found in 2–4 sponges, and (iii) the species-specific community, consisting of bacteria found in only one sponge. Using the enormous sequencing depth of pyrosequencing the diversity in each of the five sponges was extended to up to 15 different bacterial phyla per sponge with Proteobacteria and Chloroflexi being most diverse in each of the five sponges. Similarity comparison of bacteria on phylum and phylotype level revealed most similar communities in A. aerophoba and A. cavernicola and the most dissimilar community in Pseudocorticium jarrei. A surprising minimal core bacterial community was found when distribution of 97% operational taxonomic units (OTUs) was analyzed. Core, variable, and species-specific communities were comprised of 2, 26, and 72% of all OTUs, respectively. This indicates that each sponge contains a large set of unique bacteria and shares only few bacteria with other sponges. However, host species-specific bacteria are probably still closely related to each other explaining the observed similarity among bacterial communities in sponges.

Effect of Lake Trophic Status and Rooted Macrophytes on Community Composition and Abundance of Ammonia-Oxidizing Prokaryotes in Freshwater Sediments

Communities of ammonia-oxidizing archaea (AOA) and bacteria (AOB) in freshwater sediments and those in association with the root system of the macrophyte species Littorella uniflora, Juncus bulbosus, and Myriophyllum alterniflorum were compared for seven oligotrophic to mesotrophic softwater lakes and acidic heathland pools. Archaeal and bacterial ammonia monooxygenase alpha-subunit (amoA) gene diversity increased from oligotrophic to mesotrophic sites; the number of detected operational taxonomic units was positively correlated to ammonia availability and pH and negatively correlated to sediment C/N ratios. AOA communities could be grouped according to lake trophic status and pH; plant species-specific communities were not detected, and no grouping was apparent for AOB communities. Relative abundance, determined by quantitative PCR targeting amoA, was always low for AOB (<0.05% of all prokaryotes) and slightly higher for AOA in unvegetated sediment and AOA in association with M. alterniflorum (0.01 to 2%), while AOA accounted for up to 5% in the rhizospheres of L. uniflora and J. bulbosus. These results indicate that (i) AOA are at least as numerous as AOB in freshwater sediments, (ii) aquatic macrophytes with substantial release of oxygen and organic carbon into their rhizospheres, like L. uniflora and J. bulbosus, increase AOA abundance; and (iii) AOA community composition is generally determined by lake trophy, not by plant species-specific interactions.

Durchsetzungs- und Reproduktionsstrategien bei Trifolium pallescens Schreb. und Trifolium thalii Vill. : I. Untersuchungen zur Wuchsformmorphologie und Vergesellschaftung

Growth forms and community ecology of two closely related alpine Trifolium species have been studied. The species prefer distinct habitats and reproduce only by seeds: Trifolium pallescens grows on alpine screes, often in morainic areas; Trifolium thalii is predominantly to be found in subalpine-alpine pastures. This contrast in habitat behaviour was compared with the behaviour of the species along their altitudinal distribution. Observations were made in the Otztaler Alps (Tirol, Austria) and in the Montafon area (Vorarlberg, Austria). The different growth forms of these were found to correlate with the species-specific habitat and display highly adaptive plasticity along the altitudinal gradient. Trifolium pallescens is a rosette plant forming long lateral shoots which are annual with exception oft the shortened basis, while the lateral shoots of Trifolium thalii are perennial. Moreover regeneration capacity in both species is high. There are obvious relations to Trifolium repens, a closely related species of lowland pasture communities. A gradual change from generative (Trifolium pallescens, Trifolium thalii) to predominantly vegetative reproduction strategy (Trifolium repens) is obvious. The relationship between growth form, behaviour and species-specific community ecology is pointed out.