Showing papers in "The ISME Journal in 2022"

Organochlorine contamination enriches virus-encoded metabolism and pesticide degradation associated auxiliary genes in soil microbiomes

Abstract: Abstract Viruses significantly influence local and global biogeochemical cycles and help bacteria to survive in different environments by encoding various auxiliary metabolic genes (AMGs) associated with energy acquisition, stress tolerance and degradation of xenobiotics. Here we studied whether bacterial (dsDNA) virus encoded AMGs are enriched in organochlorine pesticide (OCP) contaminated soil in China and if viral AMGs include genes linked to OCP biodegradation. Using metagenomics, we found that OCP-contaminated soils displayed a lower bacterial, but higher diversity of viruses that harbored a higher relative abundance of AMGs linked to pesticide degradation and metabolism. Furthermore, the diversity and relative abundance of AMGs significantly increased along with the severity of pesticide contamination, and several biodegradation genes were identified bioinformatically in viral metagenomes. Functional assays were conducted to experimentally demonstrate that virus-encoded L-2-haloacid dehalogenase gene (L-DEX) is responsible for the degradation of L-2-haloacid pesticide precursors, improving bacterial growth at sub-inhibitory pesticide concentrations. Taken together, these results demonstrate that virus-encoded AMGs are linked to bacterial metabolism and biodegradation, being more abundant and diverse in soils contaminated with pesticides. Moreover, our findings highlight the importance of virus-encoded accessory genes for bacterial ecology in stressful environments, providing a novel avenue for using viruses in the bioremediation of contaminated soils.

Forest tree growth is linked to mycorrhizal fungal composition and function across Europe

Abstract: Abstract Most trees form symbioses with ectomycorrhizal fungi (EMF) which influence access to growth-limiting soil resources. Mesocosm experiments repeatedly show that EMF species differentially affect plant development, yet whether these effects ripple up to influence the growth of entire forests remains unknown. Here we tested the effects of EMF composition and functional genes relative to variation in well-known drivers of tree growth by combining paired molecular EMF surveys with high-resolution forest inventory data across 15 European countries. We show that EMF composition was linked to a three-fold difference in tree growth rate even when controlling for the primary abiotic drivers of tree growth. Fast tree growth was associated with EMF communities harboring high inorganic but low organic nitrogen acquisition gene proportions and EMF which form contact versus medium-distance fringe exploration types. These findings suggest that EMF composition is a strong bio-indicator of underlying drivers of tree growth and/or that variation of forest EMF communities causes differences in tree growth. While it may be too early to assign causality or directionality, our study is one of the first to link fine-scale variation within a key component of the forest microbiome to ecosystem functioning at a continental scale.

Synthetic bacterial community derived from a desert rhizosphere confers salt stress resilience to tomato in the presence of a soil microbiome

Abstract: The root bacterial microbiome is important for the general health of the plant. Additionally, it can enhance tolerance to abiotic stresses, exemplified by plant species found in extreme ecological niches like deserts. These complex microbe-plant interactions can be simplified by constructing synthetic bacterial communities or SynComs from the root microbiome. Furthermore, SynComs can be applied as biocontrol agents to protect crops against abiotic stresses such as high salinity. However, there is little knowledge on the design of a SynCom that offers a consistent protection against salt stress for plants growing in a natural and, therefore, non-sterile soil which is more realistic to an agricultural setting. Here we show that a SynCom of five bacterial strains, originating from the root of the desert plant Indigofera argentea, protected tomato plants growing in a non-sterile substrate against a high salt stress. This phenotype correlated with the differential expression of salt stress related genes and ion accumulation in tomato. Quantification of the SynCom strains indicated a low penetrance into the natural soil used as the non-sterile substrate. Our results demonstrate how a desert microbiome could be engineered into a simplified SynCom that protected tomato plants growing in a natural soil against an abiotic stress.

Small changes in rhizosphere microbiome composition predict disease outcomes earlier than pathogen density variations

Abstract: Abstract Even in homogeneous conditions, plants facing a soilborne pathogen tend to show a binary outcome with individuals either remaining fully healthy or developing severe to lethal disease symptoms. As the rhizosphere microbiome is a major determinant of plant health, we postulated that such a binary outcome may result from an early divergence in the rhizosphere microbiome assembly that may further cascade into varying disease suppression abilities. We tested this hypothesis by setting up a longitudinal study of tomato plants growing in a natural but homogenized soil infested with the soilborne bacterial pathogen Ralstonia solanacearum . Starting from an originally identical species pool, individual rhizosphere microbiome compositions rapidly diverged into multiple configurations during the plant vegetative growth. This variation in community composition was strongly associated with later disease development during the later fruiting state. Most interestingly, these patterns also significantly predicted disease outcomes 2 weeks before any difference in pathogen density became apparent between the healthy and diseased groups. In this system, a total of 135 bacterial OTUs were associated with persistent healthy plants. Five of these enriched OTUs ( Lysinibacillus , Pseudarthrobacter , Bordetella , Bacillus , and Chryseobacterium ) were isolated and shown to reduce disease severity by 30.4–100% when co-introduced with the pathogen. Overall, our results demonstrated that an initially homogenized soil can rapidly diverge into rhizosphere microbiomes varying in their ability to promote plant protection. This suggests that early life interventions may have significant effects on later microbiome states, and highlights an exciting opportunity for microbiome diagnostics and plant disease prevention.

Human gut-microbiome-derived propionate coordinates proteasomal degradation via HECTD2 upregulation to target EHMT2 in colorectal cancer

Abstract: The human microbiome plays an essential role in the human immune system, food digestion, and protection from harmful bacteria by colonizing the human intestine. Recently, although the human microbiome affects colorectal cancer (CRC) treatment, the mode of action between the microbiome and CRC remains unclear. This study showed that propionate suppressed CRC growth by promoting the proteasomal degradation of euchromatic histone-lysine N-methyltransferase 2 (EHMT2) through HECT domain E3 ubiquitin protein ligase 2 (HECTD2) upregulation. In addition, EHMT2 downregulation reduced the H3K9me2 level on the promoter region of tumor necrosis factor α-induced protein 1 (TNFAIP1) as a novel direct target of EHMT2. Subsequently, TNFAIP1 upregulation induced the apoptosis of CRC cells. Furthermore, using Bacteroides thetaiotaomicron culture medium, we confirmed EHMT2 downregulation via upregulation of HECTD2 and TNFAIP1 upregulation. Finally, we observed the synergistic effect of propionate and an EHMT2 inhibitor (BIX01294) in 3D spheroid culture models. Thus, we suggest the anticancer effects of propionate and EHMT2 as therapeutic targets for colon cancer treatment and may provide the possibility for the synergistic effects of an EHMT2 inhibitor and microbiome in CRC treatment.

The novel genus, ‘Candidatus Phosphoribacter’, previously identified as Tetrasphaera, is the dominant polyphosphate accumulating lineage in EBPR wastewater treatment plants worldwide

Abstract: The bacterial genus Tetrasphaera encompasses abundant polyphosphate accumulating organisms (PAOs) that are responsible for enhanced biological phosphorus removal (EBPR) in wastewater treatment plants. Recent analyses of genomes from pure cultures revealed that 16S rRNA genes cannot resolve the lineage, and that Tetrasphaera spp. are from several different genera within the Dermatophilaceae. Here, we examine 14 recently recovered high-quality metagenome-assembled genomes from wastewater treatment plants containing full-length 16S rRNA genes identified as Tetrasphaera, 11 of which belong to the uncultured Tetrasphaera clade 3. We find that this clade represents two distinct genera, named here Ca. Phosphoribacter and Ca. Lutibacillus, and reveal that the widely used model organism Tetrasphaera elongata is less relevant for physiological predictions of this uncultured group. Ca. Phosphoribacter incorporates species diversity unresolved at the 16S rRNA gene level, with the two most abundant and often co-occurring species encoding identical V1-V3 16S rRNA gene amplicon sequence variants but different metabolic capabilities, and possibly, niches. Both Ca. P. hodrii and Ca. P. baldrii were visualised using fluorescence in situ hybridisation (FISH), and PAO capabilities were confirmed with FISH-Raman microspectroscopy and phosphate cycling experiments. Ca. Phosphoribacter represents the most abundant former Tetrasphaera lineage and PAO in EPBR systems in Denmark and globally.

Plant neighborhood shapes diversity and reduces interspecific variation of the phyllosphere microbiome

Abstract: Microbial communities associated with plant leaf surfaces (i.e., the phyllosphere) are increasingly recognized for their role in plant health. While accumulating evidence suggests a role for host filtering of its microbiota, far less is known about how community composition is shaped by dispersal, including from neighboring plants. We experimentally manipulated the local plant neighborhood within which tomato, pepper, or bean plants were grown in a 3-month field trial. Focal plants were grown in the presence of con- or hetero-specific neighbors (or no neighbors) in a fully factorial combination. At 30-day intervals, focal plants were harvested and replaced with a new age- and species-matched cohort while allowing neighborhood plants to continue growing. Bacterial community profiling revealed that the strength of host filtering effects (i.e., interspecific differences in composition) decreased over time. In contrast, the strength of neighborhood effects increased over time, suggesting dispersal from neighboring plants becomes more important as neighboring plant biomass increases. We next implemented a cross-inoculation study in the greenhouse using inoculum generated from the field plants to directly test host filtering of microbiomes while controlling for directionality and source of dispersal. This experiment further demonstrated that focal host species, the host from which the microbiome came, and in one case the donor hosts' neighbors, contribute to variation in phyllosphere bacterial composition. Overall, our results suggest that local dispersal is a key factor in phyllosphere assembly, and that demographic factors such as nearby neighbor identity and biomass or age are important determinants of phyllosphere microbiome diversity.

Decreased efficacy of antimicrobial agents in a polymicrobial environment

Abstract: The airways of people with cystic fibrosis (CF) often harbour diverse polymicrobial communities. These airway infections can be impossible to resolve through antibiotic intervention, even though isolates of the individual species present are susceptible to the treatment when tested in vitro. In this work, we investigate how polymicrobial cultures comprised of key CF-associated pathogens respond to challenge with species-specific antimicrobial agents; colistin (targets Pseudomonas aeruginosa), fusidic acid (targets Staphylococcus aureus), and fluconazole (targets Candida albicans). We found that growth in a polymicrobial environment protects the target microorganism (sometimes by several orders of magnitude) from the effect(s) of the antimicrobial agent. This decreased antimicrobial efficacy was found to have both non-heritable (physiological) and heritable (genetic) components. Whole-genome sequencing of the colistin-resistant P. aeruginosa isolates revealed single nucleotide polymorphisms and indels in genes encoding lipopolysaccharide (LPS) biosynthesis and/or pilus biogenesis, indicating that a previously undescribed colistin resistance mechanism was in operation. This was subsequently confirmed through further genetic analyses. Our findings indicate that the polymicrobial nature of the CF airways is likely to have a significant impact on the clinical response to antimicrobial therapy.

Globally distributed mining-impacted environments are underexplored hotspots of multidrug resistance genes

Abstract: Abstract Mining is among the human activities with widest environmental impacts, and mining-impacted environments are characterized by high levels of metals that can co-select for antibiotic resistance genes (ARGs) in microorganisms. However, ARGs in mining-impacted environments are still poorly understood. Here, we conducted a comprehensive study of ARGs in such environments worldwide, taking advantage of 272 metagenomes generated from a global-scale data collection and two national sampling efforts in China. The average total abundance of the ARGs in globally distributed studied mine sites was 1572 times per gigabase, being rivaling that of urban sewage but much higher than that of freshwater sediments. Multidrug resistance genes accounted for 40% of the total ARG abundance, tended to co-occur with multimetal resistance genes, and were highly mobile (e.g. on average 16% occurring on plasmids). Among the 1848 high-quality metagenome-assembled genomes (MAGs), 85% carried at least one multidrug resistance gene plus one multimetal resistance gene. These high-quality ARG-carrying MAGs considerably expanded the phylogenetic diversity of ARG hosts, providing the first representatives of ARG-carrying MAGs for the Archaea domain and three bacterial phyla. Moreover, 54 high-quality ARG-carrying MAGs were identified as potential pathogens. Our findings suggest that mining-impacted environments worldwide are underexplored hotspots of multidrug resistance genes.

Coral holobiont cues prime Endozoicomonas for a symbiotic lifestyle

Abstract: Endozoicomonas are prevalent, abundant bacterial associates of marine animals, including corals. Their role in holobiont health and functioning, however, remains poorly understood. To identify potential interactions within the coral holobiont, we characterized the novel isolate Endozoicomonas marisrubri sp. nov. 6c and assessed its transcriptomic and proteomic response to tissue extracts of its native host, the Red Sea coral Acropora humilis. We show that coral tissue extracts stimulated differential expression of genes putatively involved in symbiosis establishment via the modulation of the host immune response by E. marisrubri 6c, such as genes for flagellar assembly, ankyrins, ephrins, and serpins. Proteome analyses revealed that E. marisrubri 6c upregulated vitamin B1 and B6 biosynthesis and glycolytic processes in response to holobiont cues. Our results suggest that the priming of Endozoicomonas for a symbiotic lifestyle involves the modulation of host immunity and the exchange of essential metabolites with other holobiont members. Consequently, Endozoicomonas may play an important role in holobiont nutrient cycling and may therefore contribute to coral health, acclimatization, and adaptation.

Routes and rates of bacterial dispersal impact surface soil microbiome composition and functioning

Abstract: Abstract Recent evidence suggests that, similar to larger organisms, dispersal is a key driver of microbiome assembly; however, our understanding of the rates and taxonomic composition of microbial dispersal in natural environments is limited. Here, we characterized the rate and composition of bacteria dispersing into surface soil via three dispersal routes (from the air above the vegetation, from nearby vegetation and leaf litter near the soil surface, and from the bulk soil and litter below the top layer). We then quantified the impact of those routes on microbial community composition and functioning in the topmost litter layer. The bacterial dispersal rate onto the surface layer was low (7900 cells/cm 2 /day) relative to the abundance of the resident community. While bacteria dispersed through all three routes at the same rate, only dispersal from above and near the soil surface impacted microbiome composition, suggesting that the composition, not rate, of dispersal influenced community assembly. Dispersal also impacted microbiome functioning. When exposed to dispersal, leaf litter decomposed faster than when dispersal was excluded, although neither decomposition rate nor litter chemistry differed by route. Overall, we conclude that the dispersal routes transport distinct bacterial communities that differentially influence the composition of the surface soil microbiome.

Nitrogen cycling and microbial cooperation in the terrestrial subsurface

Abstract: Abstract The nitrogen cycle plays a major role in aquatic nitrogen transformations, including in the terrestrial subsurface. However, the variety of transformations remains understudied. To determine how nitrogen cycling microorganisms respond to different aquifer chemistries, we sampled groundwater with varying nutrient and oxygen contents. Genes and transcripts involved in major nitrogen-cycling pathways were quantified from 55 and 26 sites, respectively, and metagenomes and metatranscriptomes were analyzed from a subset of oxic and dysoxic sites (0.3-1.1 mg/L bulk dissolved oxygen). Nitrogen-cycling mechanisms (e.g. ammonia oxidation, denitrification, dissimilatory nitrate reduction to ammonium) were prevalent and highly redundant, regardless of site-specific physicochemistry or nitrate availability, and present in 40% of reconstructed genomes, suggesting that nitrogen cycling is a core function of aquifer communities. Transcriptional activity for nitrification, denitrification, nitrite-dependent anaerobic methane oxidation and anaerobic ammonia oxidation (anammox) occurred simultaneously in oxic and dysoxic groundwater, indicating the availability of oxic-anoxic interfaces. Concurrent activity by these microorganisms indicates potential synergisms through metabolite exchange across these interfaces (e.g. nitrite and oxygen). Fragmented denitrification pathway encoding and transcription was widespread among groundwater bacteria, although a considerable proportion of associated transcriptional activity was driven by complete denitrifiers, especially under dysoxic conditions. Despite large differences in transcription, the capacity for the final steps of denitrification was largely invariant to aquifer conditions, and most genes and transcripts encoding N 2 O reductases were the atypical Sec-dependant type, suggesting energy-efficiency prioritization. Results provide insights into the capacity for cooperative relationships in groundwater communities, and the richness and complexity of metabolic mechanisms leading to the loss of fixed nitrogen.

Infection strategy and biogeography distinguish cosmopolitan groups of marine jumbo bacteriophages

Abstract: Abstract Recent research has underscored the immense diversity and key biogeochemical roles of large DNA viruses in the ocean. Although they are important constituents of marine ecosystems, it is sometimes difficult to detect these viruses due to their large size and complex genomes. This is true for “jumbo” bacteriophages, which have genome sizes >200 kbp and large capsids reaching up to 0.45 µm in diameter. In this study, we sought to assess the genomic diversity and distribution of these bacteriophages in the ocean by generating and analyzing jumbo phage genomes from metagenomes. We recover 85 marine jumbo phages that ranged in size from 201 to 498 kilobases, and we examine their genetic similarities and biogeography together with a reference database of marine jumbo phage genomes. By analyzing Tara Oceans metagenomic data, we show that although most jumbo phages can be detected in a range of different size fractions, 17 of our bins tend to be found in those greater than 0.22 µm, potentially due to their large size. Our network-based analysis of gene-sharing patterns reveals that jumbo bacteriophages belong to five genome clusters that are typified by diverse replication strategies, genomic repertoires, and potential host ranges. Our analysis of jumbo phage distributions in the ocean reveals that depth is a major factor shaping their biogeography, with some phage genome clusters occurring preferentially in either surface or mesopelagic waters, respectively. Taken together, our findings indicate that jumbo phages are widespread community members in the ocean with complex genomic repertoires and ecological impacts that warrant further targeted investigation.

Flavonoid-attracted Aeromonas sp. from the Arabidopsis root microbiome enhances plant dehydration resistance

Abstract: Abstract Flavonoids are stress-inducible metabolites important for plant-microbe interactions. In contrast to their well-known function in initiating rhizobia nodulation in legumes, little is known about whether and how flavonoids may contribute to plant stress resistance through affecting non-nodulating bacteria. Here we show that flavonoids broadly contribute to the diversity of the Arabidopsis root microbiome and preferentially attract Aeromonadaceae , which included a cultivable Aeromonas sp. H1 that displayed flavonoid-induced chemotaxis with transcriptional enhancement of flagellum biogenesis and suppression of fumarate reduction for smooth swims. Strain H1 showed multiple plant-beneficial traits and enhanced plant dehydration resistance, which required flavonoids but not through a sudden “cry-for-help” upon stress. Strain H1 boosted dehydration-induced H 2 O 2 accumulation in guard cells and stomatal closure, concomitant with synergistic induction of jasmonic acid-related regulators of plant dehydration resistance. These findings revealed a key role of flavonoids, and the underlying mechanism, in mediating plant-microbiome interactions including the bacteria-enhanced plant dehydration resistance.

Priority effects shape the structure of infant-type Bifidobacterium communities on human milk oligosaccharides

Abstract: Bifidobacteria are among the first colonizers of the infant gut, and human milk oligosaccharides (HMOs) in breastmilk are instrumental for the formation of a bifidobacteria-rich microbiota. However, little is known about the assembly of bifidobacterial communities. Here, by applying assembly theory to a community of four representative infant-gut associated Bifidobacterium species that employ varied strategies for HMO consumption, we show that arrival order and sugar consumption phenotypes significantly affected community formation. Bifidobacterium bifidum and Bifidobacterium longum subsp. infantis, two avid HMO consumers, dominate through inhibitory priority effects. On the other hand, Bifidobacterium breve, a species with limited HMO-utilization ability, can benefit from facilitative priority effects and dominates by utilizing fucose, an HMO degradant not utilized by the other bifidobacterial species. Analysis of publicly available breastfed infant faecal metagenome data showed that the observed trends for B. breve were consistent with our in vitro data, suggesting that priority effects may have contributed to its dominance. Our study highlights the importance and history dependency of initial community assembly and its implications for the maturation trajectory of the infant gut microbiota.

Heme cross-feeding can augment Staphylococcus aureus and Enterococcus faecalis dual species biofilms

Abstract: The contribution of biofilms to virulence and as a barrier to treatment is well-established for Staphylococcus aureus and Enterococcus faecalis, both nosocomial pathogens frequently isolated from biofilm-associated infections. Despite frequent co-isolation, their interactions in biofilms have not been well-characterized. We report that in combination, these two species can give rise to augmented biofilms biomass that is dependent on the activation of E. faecalis aerobic respiration. In E. faecalis, respiration requires both exogenous heme to activate the cydAB-encoded heme-dependent cytochrome bd, and the availability of O2. We determined that the ABC transporter encoded by cydDC contributes to heme import. In dual species biofilms, S. aureus provides the heme to activate E. faecalis respiration. S. aureus mutants deficient in heme biosynthesis were unable to augment biofilms whereas heme alone is sufficient to augment E. faecalis mono-species biofilms. Our results demonstrate that S. aureus-derived heme, likely in the form of released hemoproteins, promotes E. faecalis biofilm formation, and that E. faecalis gelatinase activity facilitates heme extraction from hemoproteins. This interspecies interaction and metabolic cross-feeding may explain the frequent co-occurrence of these microbes in biofilm-associated infections.

Species interactions constrain adaptation and preserve ecological stability in an experimental microbial community

Abstract: Abstract Species loss within a microbial community can increase resource availability and spur adaptive evolution. Environmental shifts that cause species loss or fluctuations in community composition are expected to become more common, so it is important to understand the evolutionary forces that shape the stability and function of the emergent community. Here we study experimental cultures of a simple, ecologically stable community of Saccharomyces cerevisiae and Lactobacillus plantarum , in order to understand how the presence or absence of a species impacts coexistence over evolutionary timescales. We found that evolution in coculture led to drastically altered evolutionary outcomes for L. plantarum , but not S. cerevisiae . Both monoculture- and co-culture-evolved L. plantarum evolved dozens of mutations over 925 generations of evolution, but only L. plantarum that had evolved in isolation from S. cerevisiae lost the capacity to coexist with S. cerevisiae . We find that the evolutionary loss of ecological stability corresponds with fitness differences between monoculture-evolved L. plantarum and S. cerevisiae and genetic changes that repeatedly evolve across the replicate populations of L. plantarum . This work shows how coevolution within a community can prevent destabilising evolution in individual species, thereby preserving ecological diversity and stability, despite rapid adaptation.

Ecological dynamics of the gut microbiome in response to dietary fiber

Abstract: Dietary fibers are generally thought to benefit intestinal health. Their impacts on the composition and metabolic function of the gut microbiome, however, vary greatly across individuals. Previous research showed that each individual's response to fibers depends on their baseline gut microbiome, but the ecology driving microbiota remodeling during fiber intake remained unclear. Here, we studied the long-term dynamics of the gut microbiome and short-chain fatty acids (SCFAs) in isogenic mice with distinct microbiota baselines fed with the fermentable fiber inulin and resistant starch compared to the non-fermentable fiber cellulose. We found that inulin produced a generally rapid response followed by gradual stabilization to new equilibria, and those dynamics were baseline-dependent. We parameterized an ecology model from the time-series data, which revealed a group of bacteria whose growth significantly increased in response to inulin and whose baseline abundance and interspecies competition explained the baseline dependence of microbiome density and community composition dynamics. Fecal levels of SCFAs, such as propionate, were associated with the abundance of inulin responders, yet inter-individual variation of gut microbiome impeded the prediction of SCFAs by machine learning models. We showed that our methods and major findings were generalizable to dietary resistant starch. Finally, we analyzed time-series data of synthetic and natural human gut microbiome in response to dietary fiber and validated the inferred interspecies interactions in vitro. This study emphasizes the importance of ecological modeling to understand microbiome responses to dietary changes and the need for personalized interventions.

Biofilm matrix cloaks bacterial quorum sensing chemoattractants from predator detection

Abstract: Microbes often secrete high levels of quorum sensing (QS) autoinducers into the environment to coordinate gene expression and biofilm formation, but risk detection and subsequent predation by bacterivorous predators. With such prominent signaling molecules acting as chemoattractants that diffuse into the environment at alarmingly high concentrations, it is unclear if bacterial cells can mask their chemical trails from predator detection. Here, we describe a microbial-based anti-detection adaptation, termed as "biofilm cloak", where the biofilm prey produced biofilm matrix exopolysaccharides that "locked" and reduced the leaching of autoinducers into the milieu, thereby concealing their trails to the detection by the bacterivorous Caenorhabditis elegans nematode. The exopolysaccharides act as common good for the non-producers to hide their autoinducers from predator detection. Deficiency in chemosensory gene odr-10 in mutant animals abrogated their ability to detect autoinducers and migrate toward their prey in a directed manner, which led to lower population growth rate of animals. Hence, restriction of bacterial communication activities to the confinements of biofilms is a novel approach for predator evasion, which plays a fundamental role in shaping ecological dynamics of microbial communities and predator-prey interactions.

Founder cell configuration drives competitive outcome within colony biofilms

Abstract: Abstract Bacteria can form dense communities called biofilms, where cells are embedded in a self-produced extracellular matrix. Exploiting competitive interactions between strains within the biofilm context can have potential applications in biological, medical, and industrial systems. By combining mathematical modelling with experimental assays, we reveal that spatial structure and competitive dynamics within biofilms are significantly affected by the location and density of the founder cells used to inoculate the biofilm. Using a species-independent theoretical framework describing colony biofilm formation, we show that the observed spatial structure and relative strain biomass in a mature biofilm comprising two isogenic strains can be mapped directly to the geographical distributions of founder cells. Moreover, we define a predictor of competitive outcome that accurately forecasts relative abundance of strains based solely on the founder cells’ potential for radial expansion. Consequently, we reveal that variability of competitive outcome in biofilms inoculated at low founder density is a natural consequence of the random positioning of founding cells in the inoculum. Extension of our study to non-isogenic strains that interact through local antagonisms, shows that even for strains with different competition strengths, a race for space remains the dominant mode of competition in low founder density biofilms. Our results, verified by experimental assays using Bacillus subtilis , highlight the importance of spatial dynamics on competitive interactions within biofilms and hence to related applications.

Ecological and genomic responses of soil microbiomes to high-severity wildfire: linking community assembly to functional potential

Abstract: Increasing wildfire severity, which is common throughout the western United States, can have deleterious effects on plant regeneration and large impacts on carbon (C) and nitrogen (N) cycling rates. Soil microbes are pivotal in facilitating these elemental cycles, so understanding the impact of increasing fire severity on soil microbial communities is critical. Here, we assess the long-term impact of high-severity fires on the soil microbiome. We find that high-severity wildfires result in a multi-decadal (>25 y) recovery of the soil microbiome mediated by concomitant differences in aboveground vegetation, soil chemistry, and microbial assembly processes. Our results depict a distinct taxonomic and functional successional pattern of increasing selection in post-fire soil microbial communities. Changes in microbiome composition corresponded with changes in microbial functional potential, specifically altered C metabolism and enhanced N cycling potential, which related to rates of potential decomposition and inorganic N availability, respectively. Based on metagenome-assembled genomes, we show that bacterial genomes enriched in our earliest site (4 y since fire) harbor distinct traits such as a robust stress response and a high potential to degrade pyrogenic, polyaromatic C that allow them to thrive in post-fire environments. Taken together, these results provide a biological basis for previously reported process rate measurements and explain the temporal dynamics of post-fire biogeochemistry, which ultimately constrains ecosystem recovery.

Broad phylogenetic and functional diversity among mixotrophic consumers of Prochlorococcus

Abstract: Small eukaryotic phytoplankton are major contributors to global primary production and marine biogeochemical cycles. Many taxa are thought to be mixotrophic, but quantitative studies of phagotrophy exist for very few. In addition, little is known about consumers of Prochlorococcus, the abundant cyanobacterium at the base of oligotrophic ocean food webs. Here we describe thirty-nine new phytoplankton isolates from the North Pacific Subtropical Gyre (Station ALOHA), all flagellates ~2-5 µm diameter, and we quantify their ability to graze Prochlorococcus. The mixotrophs are from diverse classes (dictyochophytes, haptophytes, chrysophytes, bolidophytes, a dinoflagellate, and a chlorarachniophyte), many from previously uncultured clades. Grazing ability varied substantially, with specific clearance rate (volume cleared per body volume) varying over ten-fold across isolates and six-fold across genera. Slower grazers tended to create more biovolume per prey biovolume consumed. Using qPCR we found that the haptophyte Chrysochromulina was most abundant among the isolated mixotrophs at Station ALOHA, with 76-250 cells mL-1 across depths in the upper euphotic zone (5-100 m). Our results show that within a single ecosystem the phototrophs that ingest bacteria come from many branches of the eukaryotic tree, and are functionally diverse, indicating a broad range of strategies along the spectrum from phototrophy to phagotrophy.

Metabolic adaptation to vitamin auxotrophy by leaf-associated bacteria

Abstract: Abstract Auxotrophs are unable to synthesize all the metabolites essential for their metabolism and rely on others to provide them. They have been intensively studied in laboratory-generated and -evolved mutants, but emergent adaptation mechanisms to auxotrophy have not been systematically addressed. Here, we investigated auxotrophies in bacteria isolated from Arabidopsis thaliana leaves and found that up to half of the strains have auxotrophic requirements for biotin, niacin, pantothenate and/or thiamine. We then explored the genetic basis of auxotrophy as well as traits that co-occurred with vitamin auxotrophy. We found that auxotrophic strains generally stored coenzymes with the capacity to grow exponentially for 1–3 doublings without vitamin supplementation; however, the highest observed storage was for biotin, which allowed for 9 doublings in one strain. In co-culture experiments, we demonstrated vitamin supply to auxotrophs, and found that auxotrophic strains maintained higher species richness than prototrophs upon external supplementation with vitamins. Extension of a consumer-resource model predicted that auxotrophs can utilize carbon compounds provided by other organisms, suggesting that auxotrophic strains benefit from metabolic by-products beyond vitamins.

Thermal stress triggers productive viral infection of a key coral reef symbiont

Abstract: Climate change-driven ocean warming is increasing the frequency and severity of bleaching events, in which corals appear whitened after losing their dinoflagellate endosymbionts (family Symbiodiniaceae). Viral infections of Symbiodiniaceae may contribute to some bleaching signs, but little empirical evidence exists to support this hypothesis. We present the first temporal analysis of a lineage of Symbiodiniaceae-infecting positive-sense single-stranded RNA viruses (“dinoRNAVs”) in coral colonies, which were exposed to a 5-day heat treatment (+2.1 °C). A total of 124 dinoRNAV major capsid protein gene “aminotypes” (unique amino acid sequences) were detected from five colonies of two closely related Pocillopora-Cladocopium (coral-symbiont) combinations in the experiment; most dinoRNAV aminotypes were shared between the two coral-symbiont combinations (64%) and among multiple colonies (82%). Throughout the experiment, seventeen dinoRNAV aminotypes were found only in heat-treated fragments, and 22 aminotypes were detected at higher relative abundances in heat-treated fragments. DinoRNAVs in fragments of some colonies exhibited higher alpha diversity and dispersion under heat stress. Together, these findings provide the first empirical evidence that exposure to high temperatures triggers some dinoRNAVs to switch from a persistent to a productive infection mode within heat-stressed corals. Over extended time frames, we hypothesize that cumulative dinoRNAV production in the Pocillopora-Cladocopium system could affect colony symbiotic status, for example, by decreasing Symbiodiniaceae densities within corals. This study sets the stage for reef-scale investigations of dinoRNAV dynamics during bleaching events.

Greater functional diversity and redundancy of coral endolithic microbiomes align with lower coral bleaching susceptibility

Abstract: The skeleton of reef-building coral harbors diverse microbial communities that could compensate for metabolic deficiencies caused by the loss of algal endosymbionts, i.e., coral bleaching. However, it is unknown to what extent endolith taxonomic diversity and functional potential might contribute to thermal resilience. Here we exposed Goniastrea edwardsi and Porites lutea, two common reef-building corals from the central Red Sea to a 17-day long heat stress. Using hyperspectral imaging, marker gene/metagenomic sequencing, and NanoSIMS, we characterized their endolithic microbiomes together with 15N and 13C assimilation of two skeletal compartments: the endolithic band directly below the coral tissue and the deep skeleton. The bleaching-resistant G. edwardsi was associated with endolithic microbiomes of greater functional diversity and redundancy that exhibited lower N and C assimilation than endoliths in the bleaching-sensitive P. lutea. We propose that the lower endolithic primary productivity in G. edwardsi can be attributed to the dominance of chemolithotrophs. Lower primary production within the skeleton may prevent unbalanced nutrient fluxes to coral tissues under heat stress, thereby preserving nutrient-limiting conditions characteristic of a stable coral-algal symbiosis. Our findings link coral endolithic microbiome structure and function to bleaching susceptibility, providing new avenues for understanding and eventually mitigating reef loss.

Experimental evaluation of ecological principles to understand and modulate the outcome of bacterial strain competition in gut microbiomes

Abstract: Abstract It is unclear if coexistence theory can be applied to gut microbiomes to understand their characteristics and modulate their composition. Through experiments in gnotobiotic mice with complex microbiomes, we demonstrated that strains of Akkermansia muciniphila and Bacteroides vulgatus could only be established if microbiomes were devoid of these species. Strains of A. muciniphila showed strict competitive exclusion, while B. vulgatus strains coexisted but populations were still influenced by competitive interactions. These differences in competitive behavior were reflective of genomic variation within the two species, indicating considerable niche overlap for A. muciniphila strains and a broader niche space for B. vulgatus strains. Priority effects were detected for both species as strains’ competitive fitness increased when colonizing first, which resulted in stable persistence of the A. muciniphila strain colonizing first and competitive exclusion of the strain arriving second. Based on these observations, we devised a subtractive strategy for A. muciniphila using antibiotics and showed that a strain from an assembled community can be stably replaced by another strain. By demonstrating that competitive outcomes in gut ecosystems depend on niche differences and are historically contingent, our study provides novel information to explain the ecological characteristics of gut microbiomes and a basis for their modulation.