Less Is More: Genome Reduction and the Emergence of Cooperation—Implications into the Coevolution of Microbial Communities

Organisms change to adapt to the environment in which they live, evolving with coresiding individuals. Classic Darwinism postulates the primal importance of antagonistic interactions and selfishness as a major driver of evolution, promoting an increase of genomic and organism complexities. Recently, advancements in evolutionary ecology reshaped this notion, showing how leakiness in biological functions favours the adaptive genome reduction, leading to the emergence of codependence patterns. Microbial communities are complex entities exerting a gargantuan influence on the environment and the biology of the eukaryotic hosts they are associated with. Notwithstanding, we are still far from a comprehension of the ecological and evolutionary mechanisms governing the community dynamics. Here, we review the implications of genome streamlining into the unfolding of codependence within microbial communities and how this translates to an understanding of ecological patterns underlying the emerging properties of the community.

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Lytic bacteriophage have diverse indirect effects in a synthetic cross-feeding community

The ISME Journal ◽

10.1038/s41396-019-0511-z ◽

2019 ◽

Vol 14 (1) ◽

pp. 123-134 ◽

Cited By ~ 11

Author(s):

Lisa Fazzino ◽

Jeremy Anisman ◽

Jeremy M. Chacón ◽

Richard H. Heineman ◽

William R. Harcombe

Keyword(s):

Microbial Communities ◽

Indirect Effects ◽

Community Dynamics ◽

Microbial Interactions ◽

Lytic Bacteriophage ◽

Evolutionary Mechanisms ◽

E Coli ◽

Bacterial Community Dynamics ◽

Community Growth ◽

And Function

Abstract Bacteriophage shape the composition and function of microbial communities. Yet it remains difficult to predict the effect of phage on microbial interactions. Specifically, little is known about how phage influence mutualisms in networks of cross-feeding bacteria. We mathematically modeled the impacts of phage in a synthetic microbial community in which Escherichia coli and Salmonella enterica exchange essential metabolites. In this model, independent phage attack of either species was sufficient to temporarily inhibit both members of the mutualism; however, the evolution of phage resistance facilitated yields similar to those observed in the absence of phage. In laboratory experiments, attack of S. enterica with P22vir phage followed these modeling expectations of delayed community growth with little change in the final yield of bacteria. In contrast, when E. coli was attacked with T7 phage, S. enterica, the nonhost species, reached higher yields compared with no-phage controls. T7 infection increased nonhost yield by releasing consumable cell debris, and by driving evolution of partially resistant E. coli that secreted more carbon. Our results demonstrate that phage can have extensive indirect effects in microbial communities, that the nature of these indirect effects depends on metabolic and evolutionary mechanisms, and that knowing the degree of evolved resistance leads to qualitatively different predictions of bacterial community dynamics in response to phage attack.

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

Marine Drugs ◽

10.3390/md19060298 ◽

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.

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Anthropogenic drivers of soil microbial communities and impacts on soil biological functions in agroecosystems

Global Ecology and Conservation ◽

10.1016/j.gecco.2021.e01521 ◽

2021 ◽

Vol 27 ◽

pp. e01521

Author(s):

Tony Yang ◽

Newton Lupwayi ◽

St-Arnaud Marc ◽

Kadambot H.M. Siddique ◽

Luke D. Bainard

Keyword(s):

Microbial Communities ◽

Soil Microbial Communities ◽

Biological Functions ◽

Soil Microbial ◽

Anthropogenic Drivers

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Effects of Community Versus Single Strain Inoculants on the Biocontrol of Salmonella and Microbial Community Dynamics in Alfalfa Sprouts†

Journal of Food Protection ◽

10.4315/0362-028x-68.1.40 ◽

2005 ◽

Vol 68 (1) ◽

pp. 40-48 ◽

Cited By ~ 40

Author(s):

ANABELLE MATOS ◽

JAY L. GARLAND

Keyword(s):

Microbial Community ◽

Microbial Communities ◽

Community Dynamics ◽

Community Level ◽

Microbial Consortia ◽

Single Strain ◽

Acridine Orange Staining ◽

Physiological Profiles ◽

Alfalfa Sprouts ◽

Alfalfa Seeds

Potential biological control inoculants, Pseudomonas fluorescens 2-79 and microbial communities derived from market sprouts or laboratory-grown alfalfa sprouts, were introduced into alfalfa seeds with and without a Salmonella inoculum. We examined their ability to inhibit the growth of this foodborne pathogen and assess the relative effects of the inoculants on the alfalfa microbial community structure and function. Alfalfa seeds contaminated with a Salmonella cocktail were soaked for 2 h in bacterial suspensions from each inoculant tested. Inoculated alfalfa seeds were grown for 7 days and sampled during days 1, 3, and 7. At each sampling, alfalfa sprouts were sonicated for 7 min to recover microflora from the surface, and the resulting suspensions were diluted and plated on selective and nonselective media. Total bacterial counts were obtained using acridine orange staining, and the percentage culturability was calculated. Phenotypic potential of sprout-associated microbial communities inoculated with biocontrol treatments was assessed using community-level physiological profiles based on patterns of use of 95 separate carbon sources in Biolog plates. Community-level physiological profiles were also determined using oxygen-sensitive fluorophore in BD microtiter plates to examine functional patterns in these communities. No significant differences in total and mesophilic aerobe microbial cell density or microbial richness resulting from the introduction of inoculants on alfalfa seeds with and without Salmonella were observed. P. fluorescens 2-79 exhibited the greatest reduction in the growth of Salmonella early during alfalfa growth (4.22 log at day 1), while the market sprout inoculum had the reverse effect, resulting in a maximum log reduction (5.48) of Salmonella on day 7. Community-level physiological profiles analyses revealed that market sprout communities peaked higher and faster compared with the other inoculants tested. These results suggest that different modes of actions of single versus microbial consortia biocontrol treatments may be involved.

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Visualizing Microbial Community Dynamics via a Controllable Soil Environment

mSystems ◽

10.1128/msystems.00645-19 ◽

2020 ◽

Vol 5 (1) ◽

Cited By ~ 1

Author(s):

Arunima Bhattacharjee ◽

Dusan Velickovic ◽

Thomas W. Wietsma ◽

Sheryl L. Bell ◽

Janet K. Jansson ◽

...

Keyword(s):

Soil Moisture ◽

Microbial Community ◽

Microbial Communities ◽

Community Dynamics ◽

Soil Microbial Communities ◽

Soil Microbiome ◽

Soil Core ◽

Soil Microbial ◽

Functional Relationships ◽

Microbial Community Dynamics

ABSTRACT Understanding the basic biology that underpins soil microbiome interactions is required to predict the metaphenomic response to environmental shifts. A significant knowledge gap remains in how such changes affect microbial community dynamics and their metabolic landscape at microbially relevant spatial scales. Using a custom-built SoilBox system, here we demonstrated changes in microbial community growth and composition in different soil environments (14%, 24%, and 34% soil moisture), contingent upon access to reservoirs of nutrient sources. The SoilBox emulates the probing depth of a common soil core and enables determination of both the spatial organization of the microbial communities and their metabolites, as shown by confocal microscopy in combination with mass spectrometry imaging (MSI). Using chitin as a nutrient source, we used the SoilBox system to observe increased adhesion of microbial biomass on chitin islands resulting in degradation of chitin into N-acetylglucosamine (NAG) and chitobiose. With matrix-assisted laser desorption/ionization (MALDI)-MSI, we also observed several phospholipid families that are functional biomarkers for microbial growth on the chitin islands. Fungal hyphal networks bridging different chitin islands over distances of 27 mm were observed only in the 14% soil moisture regime, indicating that such bridges may act as nutrient highways under drought conditions. In total, these results illustrate a system that can provide unprecedented spatial information about interactions within soil microbial communities as a function of changing environments. We anticipate that this platform will be invaluable in spatially probing specific intra- and interkingdom functional relationships of microbiomes within soil. IMPORTANCE Microbial communities are key components of the soil ecosystem. Recent advances in metagenomics and other omics capabilities have expanded our ability to characterize the composition and function of the soil microbiome. However, characterizing the spatial metabolic and morphological diversity of microbial communities remains a challenge due to the dynamic and complex nature of soil microenvironments. The SoilBox system, demonstrated in this work, simulates an ∼12-cm soil depth, similar to a typical soil core, and provides a platform that facilitates imaging the molecular and topographical landscape of soil microbial communities as a function of environmental gradients. Moreover, the nondestructive harvesting of soil microbial communities for the imaging experiments can enable simultaneous multiomics analysis throughout the depth of the SoilBox. Our results show that by correlating molecular and optical imaging data obtained using the SoilBox platform, deeper insights into the nature of specific soil microbial interactions can be achieved.

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Evidence for Cascades of Perturbation and Adaptation in the Metabolic Genes of Higher Termite Gut Symbionts

mBio ◽

10.1128/mbio.00223-12 ◽

2012 ◽

Vol 3 (4) ◽

Cited By ~ 7

Author(s):

Xinning Zhang ◽

Jared R. Leadbetter

Keyword(s):

Microbial Communities ◽

Convergent Evolution ◽

Last Common Ancestor ◽

Evolutionary Mechanisms ◽

Bacterial Gene ◽

Family Patterns ◽

Termite Gut ◽

Genes Encoding ◽

Gut Symbionts ◽

Extinction Events

ABSTRACTTermites and their gut microbes engage in fascinating dietary mutualisms. Less is known about how these complex symbioses have evolved after first emerging in an insect ancestor over 120 million years ago. Here we examined a bacterial gene, formate dehydrogenase (fdhF), that is key to the mutualism in 8 species of “higher” termite (members of theTermitidae, the youngest and most biomass-abundant and species-rich termite family). Patterns offdhFdiversity in the gut communities of higher termites contrasted strongly with patterns in less-derived (more-primitive) insect relatives (wood-feeding “lower” termites and roaches). We observed phylogenetic evidence for (i) the sweeping loss of several clades offdhFthat may reflect extinctions of symbiotic protozoa and, importantly, bacteria dependent on them in the last common ancestor of all higher termites and (ii) a radiation of genes from the (possibly) single allele that survived. Sweeping gene loss also resulted in (iii) the elimination of an entire clade of genes encoding selenium (Se)-independent enzymes from higher termite gut communities, perhaps reflecting behavioral or morphological innovations in higher termites that relaxed preexisting environmental limitations of Se, a dietary trace element. Curiously, several higher termite gut communities may have subsequently reencountered Se limitation, reinventing genes for Se-independent proteins via convergent evolution. Lastly, the presence of a novelfdhFlineage within litter-feeding and subterranean higher (but not other) termites may indicate recent gene “invasion” events. These results imply that cascades of perturbation and adaptation by distinct evolutionary mechanisms have impacted the evolution of complex microbial communities in a highly successful lineage of insects.IMPORTANCESince patterns of relatedness between termite hosts are broadly mirrored by the relatedness of their symbiotic gut microbiota, coevolution between hosts and gut symbionts is rightly considered an important force that has shaped dietary mutualism since its inception over 120 million years ago. Apart from that concerning lateral gene or symbiont transfer between termite gut communities (for which no evidence yet exists), there has been little discussion of alternative mechanisms impacting the evolution of mutualism. Here we provide strong gene-based evidence for past environmental perturbations creating significant upheavals that continue to reverberate throughout the gut communities of species comprising a single termite lineage. We suggest that symbiont extinction events, sweeping gene losses, evolutionary radiations, relaxation and reemergence of key nutritional pressures, convergent evolution of similar traits, and recent gene invasions have all shaped gene composition in the symbiotic gut microbial communities of higher termites, currently the most dominant and successful termite family on Earth.

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System Biology Modeling with Compositional Microbiome Data Reveals Personalized Gut Microbial Dynamics and Keystone Species

10.1101/288803 ◽

2018 ◽

Author(s):

Chenhao Li ◽

Lisa Tucker-Kellogg ◽

Niranjan Nagarajan

Keyword(s):

Microbial Communities ◽

High Throughput Sequencing ◽

Community Dynamics ◽

Keystone Species ◽

Microbial Interactions ◽

Natural Environments ◽

Sequencing Data ◽

Predator Prey ◽

Public Datasets ◽

Microbiome Data

AbstractA growing body of literature points to the important roles that different microbial communities play in diverse natural environments and the human body. The dynamics of these communities is driven by a range of microbial interactions from symbiosis to predator-prey relationships, the majority of which are poorly understood, making it hard to predict the response of the community to different perturbations. With the increasing availability of high-throughput sequencing based community composition data, it is now conceivable to directly learn models that explicitly define microbial interactions and explain community dynamics. The applicability of these approaches is however affected by several experimental limitations, particularly the compositional nature of sequencing data. We present a new computational approach (BEEM) that addresses this key limitation in the inference of generalised Lotka-Volterra models (gLVMs) by coupling biomass estimation and model inference in an expectation maximization like algorithm (BEEM). Surprisingly, BEEM outperforms state-of-the-art methods for inferring gLVMs, while simultaneously eliminating the need for additional experimental biomass data as input. BEEM’s application to previously inaccessible public datasets (due to the lack of biomass data) allowed us for the first time to analyse microbial communities in the human gut on a per individual basis, revealing personalised dynamics and keystone species.

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Corynebacterium Comparative Genomics Reveals a Role for Cobamide Sharing in the Skin Microbiome

10.1101/2020.12.02.407395 ◽

2020 ◽

Author(s):

Mary Hannah Swaney ◽

Lindsay R Kalan

Keyword(s):

Comparative Genomics ◽

Microbial Communities ◽

Community Dynamics ◽

De Novo ◽

Skin Barrier ◽

Skin Microbiome ◽

Bacterial Phyla ◽

Host Interactions ◽

Complex Interactions ◽

Associated Species

ABSTRACTThe human skin microbiome is a key player in human health, with diverse functions ranging from defense against pathogens to education of the immune system. Recent studies have begun unraveling the complex interactions within skin microbial communities, shedding light on the invaluable role that skin microorganisms have in maintaining a healthy skin barrier. While the Corynebacterium genus is a dominant taxon of the skin microbiome, relatively little is known how skin-associated Corynebacteria contribute to microbe-microbe and microbe-host interactions on the skin. Here, we performed a comparative genomics analysis of 71 Corynebacterium species from diverse ecosystems, which revealed functional differences between host- and environment-associated species. In particular, host-associated species were enriched for de novo biosynthesis of cobamides, which are a class of cofactor essential for metabolism in organisms across the tree of life but are produced by a limited number of prokaryotes. Because cobamides have been hypothesized to mediate community dynamics within microbial communities, we analyzed skin metagenomes for Corynebacterium cobamide producers, which revealed a positive correlation between cobamide producer abundance and microbiome diversity, a trait associated with skin health. We also provide the first metagenome-based assessment of cobamide biosynthesis and utilization in the skin microbiome, showing that both dominant and low abundant skin taxa encode for the de novo biosynthesis pathway and that cobamide-dependent enzymes are encoded by phylogenetically diverse taxa across the major bacterial phyla on the skin. Taken together, our results support a role for cobamide sharing within skin microbial communities, which we hypothesize mediates community dynamics.

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Microbial dynamics in a High-Arctic glacier forefield: a combined field, laboratory, and modelling approach

10.5194/bg-2016-52 ◽

2016 ◽

Author(s):

James A. Bradley ◽

Sandra Arndt ◽

Marie Šabacká ◽

Liane G. Benning ◽

Gary L. Barker ◽

...

Keyword(s):

Microbial Community ◽

Numerical Model ◽

Microbial Communities ◽

Community Dynamics ◽

Heterotrophic Bacteria ◽

High Arctic ◽

Soil Development ◽

Arctic Soils ◽

Field Laboratory ◽

Modelling Approach

Abstract. Modelling the development of soils in glacier forefields is necessary in order to assess how microbial and geochemical processes interact and shape soil development in response to glacier retreat. Furthermore, such models can help us predict microbial growth and the fate of Arctic soils in an increasingly ice-free future. Here, for the first time, we combined field sampling with laboratory analyses and numerical modelling to investigate microbial community dynamics in oligotrophic proglacial soils in Svalbard. We measured low bacterial growth rates and growth efficiencies (relative to estimates from Alpine glacier forefields), and high sensitivity to soil temperature (relative to temperate soils). We used these laboratory measurements to inform parameter values in a new numerical model and significantly refined predictions of microbial and biogeochemical dynamics of soil development over a period of roughly 120 years. The model predicted the observed accumulation of autotrophic and heterotrophic biomass. Genomic data indicated that initial microbial communities were dominated by bacteria derived from the subglacial environment, whereas older soils hosted a mixed community of autotrophic and heterotrophic bacteria. This finding was validated by the numerical model, which showed that active microbial communities play key roles in fixing and recycling carbon and nutrients. We also demonstrated the role of allochthonous carbon and microbial necromass in sustaining a pool of organic material, despite high heterotrophic activity in older soils. This combined field, laboratory and modelling approach demonstrates the value of integrated model-data studies to understand and quantify the functioning of the microbial community in an emerging High-Arctic soil ecosystem.

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Higher-order effects, continuous species interactions, and trait evolution shape microbial spatial dynamics

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2020956119 ◽

2021 ◽

Vol 119 (1) ◽

pp. e2020956119

Author(s):

Anshuman Swain ◽

Levi Fussell ◽

William F. Fagan

Keyword(s):

Microbial Diversity ◽

Species Interactions ◽

Community Dynamics ◽

Spatial Dynamics ◽

Higher Order ◽

Formation Time ◽

Community Formation ◽

Order Effects ◽

Disturbance Regimes ◽

Antagonistic Interactions

The assembly and maintenance of microbial diversity in natural communities, despite the abundance of toxin-based antagonistic interactions, presents major challenges for biological understanding. A common framework for investigating such antagonistic interactions involves cyclic dominance games with pairwise interactions. The incorporation of higher-order interactions in such models permits increased levels of microbial diversity, especially in communities in which antibiotic-producing, sensitive, and resistant strains coexist. However, most such models involve a small number of discrete species, assume a notion of pure cyclic dominance, and focus on low mutation rate regimes, none of which well represent the highly interlinked, quickly evolving, and continuous nature of microbial phenotypic space. Here, we present an alternative vision of spatial dynamics for microbial communities based on antagonistic interactions—one in which a large number of species interact in continuous phenotypic space, are capable of rapid mutation, and engage in both direct and higher-order interactions mediated by production of and resistance to antibiotics. Focusing on toxin production, vulnerability, and inhibition among species, we observe highly divergent patterns of diversity and spatial community dynamics. We find that species interaction constraints (rather than mobility) best predict spatiotemporal disturbance regimes, whereas community formation time, mobility, and mutation size best explain patterns of diversity. We also report an intriguing relationship among community formation time, spatial disturbance regimes, and diversity dynamics. This relationship, which suggests that both higher-order interactions and rapid evolution are critical for the origin and maintenance of microbial diversity, has broad-ranging links to the maintenance of diversity in other systems.

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