scholarly journals Microbial Potlatch: Cell-level adaptation of leakiness of metabolites leads to resilient symbiosis among diverse cells

2020 ◽  
Author(s):  
Jumpei F Yamagishi ◽  
Nen Saito ◽  
Kunihiko Kaneko
Keyword(s):  
Growth Rate ◽  
Microbial Communities ◽  
Cell Level ◽  
Frequency Dependent ◽  
Symbiotic Relationships ◽  
Microbial Species ◽  
Nutrient Limitations ◽  
Environmental Perturbations ◽  
Microbial Ecosystems ◽  
Diverse Species

AbstractMicrobial communities display extreme diversity, facilitated by the secretion of chemicals that can create new niches. However, it is unclear why cells often secrete even essential metabolites after evolution. By noting that cells can enhance their own growth rate by leakage of essential metabolites, we show that such leaker cells can benefit from coexistence with cells that consume the leaked chemicals in the environment. This leads to an unusual form of mutualism between “leaker” and “consumer” cells, resulting in frequency-dependent coexistence of multiple microbial species, as supported by extensive simulations. Remarkably, such symbiotic relationships generally evolve when each species adapts its leakiness to optimize its own growth rate under crowded conditions and nutrient limitations, leading to ecosystems with diverse species exchanging many metabolites with each other. In addition, such ecosystems are resilient against structural and environmental perturbations. Thus, we present a new basis for diverse, complex microbial ecosystems.

scholarly journals Adaptation of metabolite leakiness leads to symbiotic chemical exchange and to a resilient microbial ecosystem

2021 ◽  
Vol 17 (6) ◽  
pp. e1009143
Author(s):  
Jumpei F. Yamagishi ◽  
Nen Saito ◽  
Kunihiko Kaneko
Keyword(s):  
Growth Rate ◽  
Chemical Exchange ◽  
Reaction Network ◽  
Cell Level ◽  
Symbiotic Relationships ◽  
Nutrient Limitations ◽  
Environmental Perturbations ◽  
Metabolite Exchange ◽  
Asymmetric Form ◽  
Theoretical Results

Microbial communities display remarkable diversity, facilitated by the secretion of chemicals that can create new niches. However, it is unclear why cells often secrete even essential metabolites after evolution. Based on theoretical results indicating that cells can enhance their own growth rate by leaking even essential metabolites, we show that such “leaker” cells can establish an asymmetric form of mutualism with “consumer” cells that consume the leaked chemicals: the consumer cells benefit from the uptake of the secreted metabolites, while the leaker cells also benefit from such consumption, as it reduces the metabolite accumulation in the environment and thereby enables further secretion, resulting in frequency-dependent coexistence of multiple microbial species. As supported by extensive simulations, such symbiotic relationships generally evolve when each species has a complex reaction network and adapts its leakiness to optimize its own growth rate under crowded conditions and nutrient limitations. Accordingly, symbiotic ecosystems with diverse cell species that leak and exchange many metabolites with each other are shaped by cell-level adaptation of leakiness of metabolites. Moreover, the resultant ecosystems with entangled metabolite exchange are resilient against structural and environmental perturbations. Thus, we present a theory for the origin of resilient ecosystems with diverse microbes mediated by secretion and exchange of essential chemicals.

scholarly journals CaptureSeq: Hybridization-Based Enrichment of cpn60 Gene Fragments Reveals the Community Structures of Synthetic and Natural Microbial Ecosystems

2021 ◽  
Vol 9 (4) ◽  
pp. 816
Author(s):  
Matthew G. Links ◽  
Tim J. Dumonceaux ◽  
E. Luke McCarthy ◽  
Sean M. Hemmingsen ◽  
Edward Topp ◽  
...  
Keyword(s):  
Microbial Community ◽  
Microbial Communities ◽  
Dna Sequences ◽  
Pcr Amplification ◽  
Shotgun Sequencing ◽  
Natural Ecosystems ◽  
Gene Markers ◽  
Microbial Profile ◽  
Microbial Ecosystems ◽  
Pcr Targeting

Background. The molecular profiling of complex microbial communities has become the basis for examining the relationship between the microbiome composition, structure and metabolic functions of those communities. Microbial community structure can be partially assessed with “universal” PCR targeting taxonomic or functional gene markers. Increasingly, shotgun metagenomic DNA sequencing is providing more quantitative insight into microbiomes. However, both amplicon-based and shotgun sequencing approaches have shortcomings that limit the ability to study microbiome dynamics. Methods. We present a novel, amplicon-free, hybridization-based method (CaptureSeq) for profiling complex microbial communities using probes based on the chaperonin-60 gene. Molecular profiles of a commercially available synthetic microbial community standard were compared using CaptureSeq, whole metagenome sequencing, and 16S universal target amplification. Profiles were also generated for natural ecosystems including antibiotic-amended soils, manure storage tanks, and an agricultural reservoir. Results. The CaptureSeq method generated a microbial profile that encompassed all of the bacteria and eukaryotes in the panel with greater reproducibility and more accurate representation of high G/C content microorganisms compared to 16S amplification. In the natural ecosystems, CaptureSeq provided a much greater depth of coverage and sensitivity of detection compared to shotgun sequencing without prior selection. The resulting community profiles provided quantitatively reliable information about all three domains of life (Bacteria, Archaea, and Eukarya) in the different ecosystems. The applications of CaptureSeq will facilitate accurate studies of host-microbiome interactions for environmental, crop, animal and human health. Conclusions: cpn60-based hybridization enriched for taxonomically informative DNA sequences from complex mixtures. In synthetic and natural microbial ecosystems, CaptureSeq provided sequences from prokaryotes and eukaryotes simultaneously, with quantitatively reliable read abundances. CaptureSeq provides an alternative to PCR amplification of taxonomic markers with deep community coverage while minimizing amplification biases.

scholarly journals Genome Reduction and Secondary Metabolism of the Marine Sponge-Associated Cyanobacterium Leptothoe

Marine Drugs ◽  
2021 ◽  
Vol 19 (6) ◽  
pp. 298
Author(s):  
Despoina Konstantinou ◽  
Rafael V. Popin ◽  
David P. Fewer ◽  
Kaarina Sivonen ◽  
Spyros Gkelis
Keyword(s):  
Natural Products ◽  
Microbial Communities ◽  
Genomic Analysis ◽  
Gene Clusters ◽  
Marine Sponges ◽  
Genome Reduction ◽  
Extracellular Polysaccharides ◽  
Comparative Genomic ◽  
Symbiotic Relationships ◽  
Genes Encoding

Sponges form symbiotic relationships with diverse and abundant microbial communities. Cyanobacteria are among the most important members of the microbial communities that are associated with sponges. Here, we performed a genus-wide comparative genomic analysis of the newly described marine benthic cyanobacterial genus Leptothoe (Synechococcales). We obtained draft genomes from Le. kymatousa TAU-MAC 1615 and Le. spongobia TAU-MAC 1115, isolated from marine sponges. We identified five additional Leptothoe genomes, host-associated or free-living, using a phylogenomic approach, and the comparison of all genomes showed that the sponge-associated strains display features of a symbiotic lifestyle. Le. kymatousa and Le. spongobia have undergone genome reduction; they harbored considerably fewer genes encoding for (i) cofactors, vitamins, prosthetic groups, pigments, proteins, and amino acid biosynthesis; (ii) DNA repair; (iii) antioxidant enzymes; and (iv) biosynthesis of capsular and extracellular polysaccharides. They have also lost several genes related to chemotaxis and motility. Eukaryotic-like proteins, such as ankyrin repeats, playing important roles in sponge-symbiont interactions, were identified in sponge-associated Leptothoe genomes. The sponge-associated Leptothoe stains harbored biosynthetic gene clusters encoding novel natural products despite genome reduction. Comparisons of the biosynthetic capacities of Leptothoe with chemically rich cyanobacteria revealed that Leptothoe is another promising marine cyanobacterium for the biosynthesis of novel natural products.

scholarly journals A network-based approach to deciphering a dynamic microbiome’s response to a subtle perturbation

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Grace Tzun-Wen Shaw ◽  
An-Chi Liu ◽  
Chieh-Yin Weng ◽  
Yi-Chun Chen ◽  
Cheng-Yu Chen ◽  
...  
Keyword(s):  
Microbial Communities ◽  
Ecosystem Functioning ◽  
Environmental Changes ◽  
Ecosystem Dynamics ◽  
Environmental Research ◽  
Human Society ◽  
The Past ◽  
Environmental Perturbations ◽  
Before And After ◽  
Occurrence Patterns

Abstract Over the past decades, one main issue that has emerged in ecological and environmental research is how losses in biodiversity influence ecosystem dynamics and functioning, and consequently human society. Although biodiversity is a common indicator of ecosystem functioning, it is difficult to measure biodiversity in microbial communities exposed to subtle or chronic environmental perturbations. Consequently, there is a need for alternative bioindicators to detect, measure, and monitor gradual changes in microbial communities against these slight, chronic, and continuous perturbations. In this study, microbial networks before and after subtle perturbations by adding S. acidaminiphila showed diverse topological niches and 4-node motifs in which microbes with co-occurrence patterns played the central roles in regulating and adjusting the intertwined relationships among microorganisms in response to the subtle environmental changes. This study demonstrates that microbial networks are a good bioindicator for chronic perturbation and should be applied in a variety of ecological investigations.

scholarly journals Time-series genome-centric analysis unveils bacterial response to operational disturbance in activated sludge

2019 ◽  
Author(s):  
María Victoria Pérez ◽  
Leandro D. Guerrero ◽  
Esteban Orellana ◽  
Eva L. Figuerola ◽  
Leonardo Erijman
Keyword(s):  
Growth Rate ◽  
Time Series ◽  
Wastewater Treatment ◽  
Activated Sludge ◽  
Microbial Communities ◽  
Wastewater Treatment Plant ◽  
Treatment Plant ◽  
Operating Conditions ◽  
The Face

ABSTRACTUnderstanding ecosystem response to disturbances and identifying the most critical traits for the maintenance of ecosystem functioning are important goals for microbial community ecology. In this study, we used 16S rRNA amplicon sequencing and metagenomics to investigate the assembly of bacterial populations in a full-scale municipal activated sludge wastewater treatment plant over a period of three years, including a period of nine month of disturbance, characterized by short-term plant shutdowns. Following the reconstruction of 173 metagenome-assembled genomes, we assessed the functional potential, the number of rRNA gene operons and thein situgrowth rate of microorganisms present throughout the time series. Operational disturbances caused a significant decrease in bacteria with a single copy of the ribosomal RNA (rrn) operon. Despite only moderate differences in resource availability, replication rates were distributed uniformly throughout time, with no differences between disturbed and stable periods. We suggest that the length of the growth lag phase, rather than the growth rate, as the primary driver of selection under disturbed conditions. Thus, the system could maintain its function in the face of disturbance by recruiting bacteria with the capacity to rapidly resume growth under unsteady operating conditions.IMPORTANCEIn this work we investigated the response of microbial communities to disturbances in a full-scale activated sludge wastewater treatment plant over a time-scale that included periods of stability and disturbance. We performed a genome-wide analysis, which allowed us the direct estimation of specific cellular traits, including the rRNA operon copy number and the in situ growth rate of bacteria. This work builds upon recent efforts to incorporate growth efficiency for the understanding of the physiological and ecological processes shaping microbial communities in nature. We found evidence that would suggest that activated sludge could maintain its function in the face of disturbance by recruiting bacteria with the capacity to rapidly resume growth under unsteady operating conditions. This paper provides relevant insights into wastewater treatment process, and may also reveal a key role for growth traits in the adaptive response of bacteria to unsteady environmental conditions.

scholarly journals Synthetic microbial ecosystems: an exciting tool to understand and apply microbial communities

2013 ◽  
Vol 16 (6) ◽  
pp. 1472-1481 ◽  
Author(s):  
Karen De Roy ◽  
Massimo Marzorati ◽  
Pieter Van den Abbeele ◽  
Tom Van de Wiele ◽  
Nico Boon
Keyword(s):  
Microbial Communities ◽  
Microbial Ecosystems

scholarly journals Heteroresistance at the Single-Cell Level: Adapting to Antibiotic Stress through a Population-Based Strategy and Growth-Controlled Interphenotypic Coordination

mBio ◽  
2014 ◽  
Vol 5 (1) ◽  
Author(s):  
Xiaorong Wang ◽  
Yu Kang ◽  
Chunxiong Luo ◽  
Tong Zhao ◽  
Lin Liu ◽  
...  
Keyword(s):  
Growth Rate ◽  
Single Cell ◽  
Task Allocation ◽  
Bacterial Population ◽  
Population Based ◽  
Phenotypic Heterogeneity ◽  
Single Cell Level ◽  
Bacterial Survival ◽  
Cell Level ◽  
Resistant Cells

ABSTRACT Heteroresistance refers to phenotypic heterogeneity of microbial clonal populations under antibiotic stress, and it has been thought to be an allocation of a subset of “resistant” cells for surviving in higher concentrations of antibiotic. The assumption fits the so-called bet-hedging strategy, where a bacterial population “hedges” its “bet” on different phenotypes to be selected by unpredicted environment stresses. To test this hypothesis, we constructed a heteroresistance model by introducing a bla CTX-M-14 gene (coding for a cephalosporin hydrolase) into a sensitive Escherichia coli strain. We confirmed heteroresistance in this clone and that a subset of the cells expressed more hydrolase and formed more colonies in the presence of ceftriaxone (exhibited stronger “resistance”). However, subsequent single-cell-level investigation by using a microfluidic device showed that a subset of cells with a distinguishable phenotype of slowed growth and intensified hydrolase expression emerged, and they were not positively selected but increased their proportion in the population with ascending antibiotic concentrations. Therefore, heteroresistance—the gradually decreased colony-forming capability in the presence of antibiotic—was a result of a decreased growth rate rather than of selection for resistant cells. Using a mock strain without the resistance gene, we further demonstrated the existence of two nested growth-centric feedback loops that control the expression of the hydrolase and maximize population growth in various antibiotic concentrations. In conclusion, phenotypic heterogeneity is a population-based strategy beneficial for bacterial survival and propagation through task allocation and interphenotypic collaboration, and the growth rate provides a critical control for the expression of stress-related genes and an essential mechanism in responding to environmental stresses. IMPORTANCE Heteroresistance is essentially phenotypic heterogeneity, where a population-based strategy is thought to be at work, being assumed to be variable cell-to-cell resistance to be selected under antibiotic stress. Exact mechanisms of heteroresistance and its roles in adaptation to antibiotic stress have yet to be fully understood at the molecular and single-cell levels. In our study, we have not been able to detect any apparent subset of “resistant” cells selected by antibiotics; on the contrary, cell populations differentiate into phenotypic subsets with variable growth statuses and hydrolase expression. The growth rate appears to be sensitive to stress intensity and plays a key role in controlling hydrolase expression at both the bulk population and single-cell levels. We have shown here, for the first time, that phenotypic heterogeneity can be beneficial to a growing bacterial population through task allocation and interphenotypic collaboration other than partitioning cells into different categories of selective advantage.

scholarly journals Spatial heterogeneity of the shorebird gastrointestinal microbiome

2020 ◽  
Vol 7 (1) ◽  
pp. 191609
Author(s):  
Kirsten Grond ◽  
Hannah Guilani ◽  
Sarah M. Hird
Keyword(s):  
Microbial Communities ◽  
Large Intestine ◽  
Alpha Diversity ◽  
Source Tracking ◽  
Similar Species ◽  
Gastrointestinal Microbiome ◽  
Semipalmated Sandpiper ◽  
Microbial Ecosystems ◽  
Genus Richness ◽  
Intestine Microbiome

The gastrointestinal tract (GIT) consists of connected structures that vary in function and physiology, and different GIT sections potentially provide different habitats for microorganisms. Birds possess unique GIT structures, including the oesophagus, proventriculus, gizzard, small intestine, caeca and large intestine. To understand birds as hosts of microbial ecosystems, we characterized the microbial communities in six sections of the GIT of two shorebird species, the Dunlin and Semipalmated Sandpiper, identified potential host species effects on the GIT microbiome and used microbial source tracking to determine microbial origin throughout the GIT. The upper three GIT sections had higher alpha diversity and genus richness compared to the lower sections, and microbial communities in the upper GIT showed no clustering. The proventriculus and gizzard microbiomes primarily originated from upstream sections, while the majority of the large intestine microbiome originated from the caeca. The heterogeneity of the GIT sections shown in our study urges caution in equating data from faeces or a single GIT component to the entire GIT microbiome but confirms that ecologically similar species may share many attributes in GIT microbiomes.

Pathogen identification in prostate cancer biopsies using transcriptome sequencing.

2017 ◽  
Vol 35 (15_suppl) ◽  
pp. e16545-e16545
Author(s):  
Carisa M Shah ◽  
Rohan Bareja ◽  
Olivier Elemento
Keyword(s):  
Prostate Cancer ◽  
Bone Metastases ◽  
Microbial Communities ◽  
Rna Sequencing ◽  
Metastatic Prostate Cancer ◽  
Microbial Pathogens ◽  
Sequencing Data ◽  
Streptomyces Species ◽  
Microbial Species ◽  
Tumor Biopsies

e16545 Background: Tumor biopsies may frequently be associated with microbial species due to proximity with microbial communities or due to contamination during tissue processing. We examined sequencing data from tumor biopsies to explore the tumor-associated microbiome in prostate cancer. Methods: Patients were enrolled in a prospective Precision Medicine study to evaluate genomic alterations based on freshly obtained tissue biopsies. Total RNA was prepared for RNA sequencing using the standard Illumina mRNA sample preparation protocol. Paired-end RNA-sequencing at read lengths of 50 or 51 bp was performed with the HiSeq 2000 (Illumina). A total of ~268 million paired-end reads were generated, corresponding to 27 billion bases. Kraken and FusionCatcher were used to identify the metagenome that maps to microbial species. R was used to analyze the microbial pathogens and to create a heatmap of microbial abundance. We focused our analysis on prostate cancer. Results: From 1/30/2013 to 12/16/15, 83 patients with urothelial cancers were identified, of which 32 patients with prostate cancer (n = 23 from primary tumor, n = 9 metastatic prostate cancer) were sequenced. Of the 9 metastatic samples, 5 were metastatic prostate cancer to bone, 4 were other metastases. A giant cell tumor of bone was used as a control. The metagenome was identified and mapped to the Kraken pathogen database. 43 unique pathogens characterized the microbiome associated with prostate cancer, including Streptomyces species, Acinetobacter baumannii, Enterobacteriaceae, and Corynebacterium species. The most prevalent species in prostate cancer bone metastases were also the most prevalent in primary prostate tumors. Prostate cancer bone metastases clustered separately from the primary prostate cancer samples, the other metastases, and primary bone cancer. Conclusions: We have identified a putative microbiome signature associated with prostate cancer. Prostate cancer bone metastases appear to cluster separately from prostate cancer, suggesting a non-random association with microbial communities. Ongoing work is looking to (1) validate microbial association using orthogonal analyses and (2) determine the exact origin of the signature.

scholarly journals Facility-Specific “House” Microbiome Drives Microbial Landscapes of Artisan Cheesemaking Plants

2013 ◽  
Vol 79 (17) ◽  
pp. 5214-5223 ◽  
Author(s):  
Nicholas A. Bokulich ◽  
David A. Mills
Keyword(s):  
Microbial Communities ◽  
High Throughput Sequencing ◽  
Microbial Consortia ◽  
True Nature ◽  
Specific Product ◽  
Site Specific ◽  
Content Type ◽  
Microbial Ecosystems ◽  
Spatial Diversification ◽  
Regional Product

ABSTRACTCheese fermentations involve the growth of complex microbial consortia, which often originate in the processing environment and drive the development of regional product qualities. However, the microbial milieus of cheesemaking facilities are largely unexplored and the true nature of the fermentation-facility relationship remains nebulous. Thus, a high-throughput sequencing approach was employed to investigate the microbial ecosystems of two artisanal cheesemaking plants, with the goal of elucidating how the processing environment influences microbial community assemblages. Results demonstrate that fermentation-associated microbes dominated most surfaces, primarilyDebaryomycesandLactococcus, indicating that establishment of these organisms on processing surfaces may play an important role in microbial transfer, beneficially directing the course of sequential fermentations. Environmental organisms detected in processing environments dominated the surface microbiota of washed-rind cheeses maturing in both facilities, demonstrating the importance of the processing environment for populating cheese microbial communities, even in inoculated cheeses. Spatial diversification within both facilities reflects the functional adaptations of microbial communities inhabiting different surfaces and the existence of facility-specific “house” microbiota, which may play a role in shaping site-specific product characteristics.

Sign in / Sign up

Export Citation Format

Share Document