Metabolic dissimilarity determines the establishment of cross-feeding interactions in bacteria

AbstractThe exchange of metabolites among different bacterial genotypes is key for determining the structure and function of microbial communities. However, the factors that govern the establishment of these cross-feeding interactions remain poorly understood. While kin selection theory predicts that individuals should direct benefits preferentially to close relatives, the potential benefits resulting from a metabolic exchange may be larger for more distantly related species. Here we distinguish between these two possibilities by performing pairwise cocultivation experiments between auxotrophic recipients and 25 species of potential amino acid donors. Auxotrophic recipients were able to grow in the vast majority of pairs tested (78%), suggesting that metabolic cross-feeding interactions are readily established. Strikingly, both the phylogenetic distance between donor and recipient as well as the dissimilarity of their metabolic networks was positively associated with the growth of auxotrophic recipients. Finally, this result was corroborated in an in-silico analysis of a co-growth of species from a gut microbial community. Together, these findings suggest metabolic cross-feeding interactions are more likely to establish between strains that are metabolically more dissimilar. Thus, our work identifies a new rule of microbial community assembly, which can help predict, understand, and manipulate natural and synthetic microbial systems.SignificanceMetabolic cross-feeding is critical for determining the structure and function of natural microbial communities. However, the rules that determine the establishment of these interactions remain poorly understood. Here we systematically analyze the propensity of different bacterial species to engage in unidirectional cross-feeding interactions. Our results reveal that synergistic growth was prevalent in the vast majority of cases analyzed. Moreover, both phylogenetic and metabolic dissimilarity between donors and recipients favored a successful establishment of metabolite exchange interactions. This work identifies a new rule of microbial community assembly that can help predict, understand, and manipulate microbial communities for diverse applications.

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A conceptual framework for the phylogenetically constrained assembly of microbial communities

Microbiome ◽

10.1186/s40168-019-0754-y ◽

2019 ◽

Vol 7 (1) ◽

Cited By ~ 5

Author(s):

Daniel Aguirre de Cárcer

Keyword(s):

Microbial Community ◽

Microbial Communities ◽

Community Assembly ◽

Phylogenetic Signal ◽

A Priori ◽

Amplicon Sequencing ◽

Bioinformatic Analysis ◽

Microbial Ecosystems ◽

And Function ◽

Microbial Community Assembly

Abstract Microbial communities play essential and preponderant roles in all ecosystems. Understanding the rules that govern microbial community assembly will have a major impact on our ability to manage microbial ecosystems, positively impacting, for instance, human health and agriculture. Here, I present a phylogenetically constrained community assembly principle grounded on the well-supported facts that deterministic processes have a significant impact on microbial community assembly, that microbial communities show significant phylogenetic signal, and that microbial traits and ecological coherence are, to some extent, phylogenetically conserved. From these facts, I derive a few predictions which form the basis of the framework. Chief among them is the existence, within most microbial ecosystems, of phylogenetic core groups (PCGs), defined as discrete portions of the phylogeny of varying depth present in all instances of the given ecosystem, and related to specific niches whose occupancy requires a specific phylogenetically conserved set of traits. The predictions are supported by the recent literature, as well as by dedicated analyses. Integrating the effect of ecosystem patchiness, microbial social interactions, and scale sampling pitfalls takes us to a comprehensive community assembly model that recapitulates the characteristics most commonly observed in microbial communities. PCGs’ identification is relatively straightforward using high-throughput 16S amplicon sequencing, and subsequent bioinformatic analysis of their phylogeny, estimated core pan-genome, and intra-group co-occurrence should provide valuable information on their ecophysiology and niche characteristics. Such a priori information for a significant portion of the community could be used to prime complementing analyses, boosting their usefulness. Thus, the use of the proposed framework could represent a leap forward in our understanding of microbial community assembly and function.

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Deterministic Selection Dominates Microbial Community Assembly in Termite Mounds Across a Large Spatial Area

10.21203/rs.3.rs-34782/v1 ◽

2020 ◽

Author(s):

Qing-Lin Chen ◽

Hang-Wei Hu ◽

Zhen-Zhen Yan ◽

Chao-Yu Li ◽

Bao-Anh Thi Nguyen ◽

...

Keyword(s):

Microbial Community ◽

Stochastic Processes ◽

Microbial Communities ◽

Fungal Community ◽

Community Assembly ◽

Distance Decay ◽

Termite Mounds ◽

Deterministic Processes ◽

Microbial Community Assembly

Abstract Background: Termites are ubiquitous insects in tropical and subtropical habitats, where they construct massive mounds from soil, their saliva and excreta. Termite mounds harbor an enormous amount of microbial inhabitants, which regulate multiple ecosystem functions such as mitigating methane emissions and increasing ecosystem resistance to climate change. However, we lack a mechanistic understanding about the role of termite mounds in modulating the microbial community assembly processes, which are essential to unravel the biological interactions of soil fauna and microorganisms, the major components of soil food webs. We conducted a large-scale survey across a >1500 km transect in northern Australia to investigate biogeographical patterns of bacterial and fungal community in 134 termite mounds and the relative importance of deterministic versus stochastic processes in microbial community assembly. Results: Microbial alpha (number of phylotypes) and beta (changes in bacterial and fungal community composition) significantly differed between termite mounds and surrounding soils. Microbial communities in termite mounds exhibited a significant distance-decay pattern, and fungal communities had a stronger distance-decay relationship (slope = -1.91) than bacteria (slope = -0.21). Based on the neutral community model (fitness < 0.7) and normalized stochasticity ratio index (NST) with a value below the 50% boundary point, deterministic selection, rather than stochastic forces, predominated the microbial community assembly in termite mounds. Deterministic processes exhibited significantly weaker impacts on bacteria (NST = 45.23%) than on fungi (NST = 33.72%), probably due to the wider habitat niche breadth and higher potential migration rate of bacteria. The abundance of antibiotic resistance genes (ARGs) was negatively correlated with bacterial/fungal biomass ratios, indicating that ARG content might be an important biotic factor that drove the biogeographic pattern of microbial communities in termite mounds. Conclusions: Deterministic processes play a more important role than stochastic processes in shaping the microbial community assembly in termite mounds, an unique habitat ubiquitously distributed in tropical and subtropical ecosystems. An improved understanding of the biogeographic patterns of microorganisms in termite mounds is crucial to decipher the role of soil faunal activities in shaping microbial community assembly, with implications for their mediated ecosystems functions and services.

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Hill-based Dissimilarity Indices and Null Models for Analysis of Microbial Community Assembly

10.21203/rs.3.rs-33130/v1 ◽

2020 ◽

Author(s):

Oskar Modin ◽

Raquel Liebana ◽

Soroush Saheb-Alam ◽

Britt-Marie Wilén ◽

Carolina Suarez ◽

...

Keyword(s):

Microbial Community ◽

Microbial Communities ◽

Community Assembly ◽

Null Model ◽

Amplicon Sequencing ◽

Null Models ◽

Marker Genes ◽

Experimental Systems ◽

Microbial Community Assembly ◽

The Impact

Abstract Background: High-throughput amplicon sequencing of marker genes, such as the 16S rRNA gene in Bacteria and Archaea, provides a wealth of information about the composition of microbial communities. To quantify differences between samples and draw conclusions about factors affecting community assembly, dissimilarity indices are typically used. However, results are subject to several biases and data interpretation can be challenging. The Jaccard and Bray-Curtis indices, which are often used to quantify taxonomic dissimilarity, are not necessarily the most logical choices. Instead, we argue that Hill-based indices, which make it possible to systematically investigate the impact of relative abundance on dissimilarity, should be used for robust analysis of data. In combination with a null model, mechanisms of microbial community assembly can be analyzed. Here, we also introduce a new software, qdiv, which enables rapid calculations of Hill-based dissimilarity indices in combination with null models.Results: Using amplicon sequencing data from two experimental systems, aerobic granular sludge (AGS) reactors and microbial fuel cells (MFC), we show that the choice of dissimilarity index can have considerable impact on results and conclusions. High dissimilarity between replicates because of random sampling effects make incidence-based indices less suited for identifying differences between groups of samples. Determining a consensus table based on count tables generated with different bioinformatic pipelines reduced the number of low-abundant, potentially spurious amplicon sequence variants (ASVs) in the data sets, which led to lower dissimilarity between replicates. Analysis with a combination of Hill-based indices and a null model allowed us to show that different ecological mechanisms acted on different fractions of the microbial communities in the experimental systems.Conclusions: Hill-based indices provide a rational framework for analysis of dissimilarity between microbial community samples. In combination with a null model, the effects of deterministic and stochastic community assembly factors on taxa of different relative abundances can be systematically investigated. Calculations of Hill-based dissimilarity indices in combination with a null model can be done in qdiv, which is freely available as a Python package (https://github.com/omvatten/qdiv). In qdiv, a consensus table can also be determined from several count tables generated with different bioinformatic pipelines.

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Structure and function of the bacterial and fungal gut flora of Neotropical butterflies

10.1101/128884 ◽

2017 ◽

Cited By ~ 3

Author(s):

Alison Ravenscraft ◽

Michelle Berry ◽

Tobin Hammer ◽

Kabir Peay ◽

Carol Boggs

Keyword(s):

Amino Acids ◽

Microbial Communities ◽

Bacterial Species ◽

Microbial Community Composition ◽

Structure And Function ◽

Feeding Guilds ◽

Gut Flora ◽

Microbial Composition ◽

Host Diet ◽

And Function

AbstractThe relationship between animals and their gut flora is simultaneously one of the most common and most complex symbioses on Earth. Despite its ubiquity, our understanding of this invisible but often critical relationship is still in its infancy. We employed adult Neotropical butterflies as a study system to ask three questions: First, how does gut microbial community composition vary across host individuals, species and dietary guilds? Second, how do gut flora compare to food microbial communities? Finally, are gut flora functionally adapted to the chemical makeup of host foods? To answer these questions we captured nearly 300 Costa Rican butterflies representing over 50 species, six families and two feeding guilds: frugivores and nectivores. We characterized the bacteria and fungi in guts, wild fruits and wild nectars via amplicon sequencing and assessed the catabolic abilities of the gut flora via culture-based assays.Gut communities were distinct from food communities, suggesting that the gut environment acts as a strong filter on potential colonists. Nevertheless, gut flora varied widely among individuals and species. On average, a pair of butterflies shared 21% of their bacterial species and 6% of their fungi. Host species explained 25-30% of total variation in microbial communities while host diet explained 4%. However, diet was still relevant at the individual microbe level—half of the most abundant microbial species differed in abundance between frugivores and nectivores. Diet was also related to the functional profile of gut flora: compared to frugivores, nectivores’ gut flora exhibited increased catabolism of sugars and sugar alcohols and decreased catabolism of amino acids, carboxylic acids and dicarboxylic acids. Since fermented juice contains more amino acids and less sugar than nectar, it appears that host diet filters the gut flora by favoring microbes that digest compounds abundant in foods.By quantifying the degree to which gut communities vary among host individuals, species and dietary guilds and evaluating how gut microbial composition and catabolic potential are related to host diet, this study deepens our understanding of the structure and function of one of the most complex and ubiquitous symbioses in the animal kingdom.

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Predation by protists influences the temperature response of microbial communities

10.1101/2021.04.08.439073 ◽

2021 ◽

Author(s):

Jennifer D Rocca ◽

Andrea Yammine ◽

Marie Simonin ◽

Jean Gibert

Keyword(s):

Community Structure ◽

Microbial Community ◽

Microbial Biomass ◽

Microbial Communities ◽

Microbial Community Structure ◽

Temperature Response ◽

Global Carbon Cycle ◽

Structure And Function ◽

And Function ◽

Global Carbon

Temperature strongly influences microbial community structure and function, which in turn contributes to the global carbon cycle that can fuel further warming. Recent studies suggest that biotic interactions amongst microbes may play an important role in determining the temperature responses of these communities. However, how microbial predation regulates these communities under future climates is still poorly understood. Here we assess whether predation by one of the most important bacterial consumers globally, protists, influences the temperature response of a freshwater microbial community structure and function. To do so, we exposed these microbial communities to two cosmopolitan species of protists at two different temperatures, in a month-long microcosm experiment. While microbial biomass and respiration increased with temperature due to shifts in microbial community structure, these responses changed over time and in the presence of protist predators. Protists influenced microbial biomass and function through effects on community structure, and predation actually reduced microbial respiration rate at elevated temperature. Indicator species and threshold indicator taxa analyses showed that these predation effects were mostly determined by phylum-specific bacterial responses to protist density and cell size. Our study supports previous findings that temperature is an important driver of microbial communities, but also demonstrates that predation can mediate these responses to warming, with important consequences for the global carbon cycle and future warming.

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Soil and sediment microbial structure and function in intermittent stream corridors after a decade of catchment succession

10.5194/egusphere-egu2020-4952 ◽

2020 ◽

Author(s):

Jose Schreckinger ◽

Aline Frossard ◽

Linda Gerull ◽

Mark O. Gessner ◽

Michael Mutz

Keyword(s):

Microbial Community ◽

Microbial Communities ◽

Vegetation Cover ◽

Structure And Function ◽

Grass Species ◽

Microbial Structure ◽

Small Streams ◽

Northeastern Germany ◽

And Function ◽

Soil And Sediment

<p>Large-scale resource exploitation by open-cast mining severely alters landscapes and impairs key ecosystem properties such as soil and sediment structure and function. Understanding the ecological recovery processes starting from an initially bare landscape generated by destructive land-use is extremely limited. Here we took advantage of a 6-ha experimental catchment to assess microbial community structure and function in soils and stream sediments after 3 and 13 years of catchment succession. The catchment (Chicken Creek) was created in 2005 by depositing quaternary sands from a lignite mine forefield in northeastern Germany and has since been left to develop under undisturbed conditions. In the initial stage, 3 years after catchment construction, rills and small streams had formed and the sparse vegetation cover mainly consisted of forbs. Over the next 10 years, the geomorphology, hydrology, and vegetation structure underwent a major transformation. A nearly full vegetation cover established, including various tree, shrub and grass species. Increased evaporation lowered the shallow groundwater table and led to stream intermittency. These changes were accompanied by large modifications in the structure and function of the microbial communities in sediments and soils. Initially, microbial structure and function were strikingly disconnected, whereas linkages had established 10 years later, although some functions still remained disconnected. Potential enzymatic activities increased vastly over the course of 10 years and also became much less variable across seasons. Cyanobacteria, predominant in soils and sediments during the early successional stage, declined to become a minor component of the microbial community. Moreover, despite distinct flow intermittency of the streams, microbial structure and function distinctly differed between sediments and adjacent soils. These results demonstrate a rapid succession of microbial communities during a decade of ecosystem development, suggesting that undisturbed succession is a feasible catchment restoration strategy.</p>

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Disturbance and recovery: a synthesis of microbial community reassembly following disturbance across realms

10.22541/au.163818947.78737764/v1 ◽

2021 ◽

Author(s):

Stephanie Jurburg ◽

Shane Blowes ◽

Ashley Shade ◽

Nico Eisenhauer ◽

Jonathan Chase

Keyword(s):

Time Series ◽

Microbial Community ◽

Microbial Communities ◽

Community Composition ◽

Community Assembly ◽

Disturbance And Recovery ◽

Microbial Community Assembly ◽

Community Reassembly ◽

Over Time

Disturbances alter the diversity and composition of microbial communities, but whether microbiomes from different environments exhibit similar degrees of resistance or rates of recovery has not been evaluated. Here, we synthesized 86 time series of disturbed mammalian, aquatic, and soil microbiomes to examine how the recovery of microbial richness and community composition differed after disturbance. We found no general patterns in compositional variance (i.e., dispersion) in any microbiomes over time. Only mammalian microbiomes consistently exhibited decreases in richness following disturbance. Importantly, they tended to recover this richness, but not their composition, over time. In contrast, aquatic microbiomes tended to diverge from their pre-disturbance composition following disturbance. By synthesizing microbiome responses across environments, our study aids in the reconciliation of disparate microbial community assembly frameworks, and highlights the role of the environment in microbial community reassembly following disturbance.

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Oil and Gas Wastewater Components Alter Streambed Microbial Community Structure and Function

Frontiers in Microbiology ◽

10.3389/fmicb.2021.752947 ◽

2021 ◽

Vol 12 ◽

Author(s):

Denise M. Akob ◽

Adam C. Mumford ◽

Andrea Fraser ◽

Cassandra R. Harris ◽

William H. Orem ◽

...

Keyword(s):

Community Structure ◽

Microbial Community ◽

West Virginia ◽

Hydraulic Fracturing ◽

Microbial Communities ◽

Microbial Community Structure ◽

Oil And Gas ◽

Structure And Function ◽

Underground Injection ◽

And Function

The widespread application of directional drilling and hydraulic fracturing technologies expanded oil and gas (OG) development to previously inaccessible resources. A single OG well can generate millions of liters of wastewater, which is a mixture of brine produced from the fractured formations and injected hydraulic fracturing fluids (HFFs). With thousands of wells completed each year, safe management of OG wastewaters has become a major challenge to the industry and regulators. OG wastewaters are commonly disposed of by underground injection, and previous research showed that surface activities at an Underground Injection Control (UIC) facility in West Virginia affected stream biogeochemistry and sediment microbial communities immediately downstream from the facility. Because microbially driven processes can control the fate and transport of organic and inorganic components of OG wastewater, we designed a series of aerobic microcosm experiments to assess the influence of high total dissolved solids (TDS) and two common HFF additives—the biocide 2,2-dibromo-3-nitrilopropionamide (DBNPA) and ethylene glycol (an anti-scaling additive)—on microbial community structure and function. Microcosms were constructed with sediment collected upstream (background) or downstream (impacted) from the UIC facility in West Virginia. Exposure to elevated TDS resulted in a significant decrease in aerobic respiration, and microbial community analysis following incubation indicated that elevated TDS could be linked to the majority of change in community structure. Over the course of the incubation, the sediment layer in the microcosms became anoxic, and addition of DBNPA was observed to inhibit iron reduction. In general, disruptions to microbial community structure and function were more pronounced in upstream and background sediment microcosms than in impacted sediment microcosms. These results suggest that the microbial community in impacted sediments had adapted following exposure to OG wastewater releases from the site. Our findings demonstrate the potential for releases from an OG wastewater disposal facility to alter microbial communities and biogeochemical processes. We anticipate that these studies will aid in the development of useful models for the potential impact of UIC disposal facilities on adjoining surface water and shallow groundwater.

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A quantitative framework reveals the ecological drivers of grassland soil microbial community assembly in response to warming

10.1101/2020.02.22.960872 ◽

2020 ◽

Author(s):

Daliang Ning ◽

Mengting Yuan ◽

Linwei Wu ◽

Ya Zhang ◽

Xue Guo ◽

...

Keyword(s):

Microbial Community ◽

Microbial Communities ◽

Community Assembly ◽

Soil Microbial Community ◽

Null Model ◽

Relative Importance ◽

Community Based ◽

Grassland Soil ◽

Soil Microbial ◽

Microbial Community Assembly

AbstractUnraveling the drivers controlling community assembly is a central issue in ecology. Selection, dispersal, diversification and drift are conceptually accepted as major community assembly processes. Defining their relative importance in governing biodiversity is compellingly needed, but very challenging. Here, we present a novel framework to quantitatively infer community assembly mechanisms by phylogenetic bin-based null model analysis (iCAMP). Our results with simulated microbial communities showed that iCAMP had high accuracy (0.93 - 0.99), precision (0.80 - 0.94), sensitivity (0.82 - 0.94), and specificity (0.95 - 0.98), which were 10-160% higher than those from the entire community-based approach. Applying it to grassland microbial communities in response to experimental warming, our analysis showed that homogeneous selection (38%) and “drift” (59%) played dominant roles in controlling grassland soil microbial community assembly. Interestingly, warming enhanced homogeneous selection, but decreased “drift” over time. Warming-enhanced selection was primarily imposed on Bacillales in Firmicutes, which were strengthened by increased drought and reduced plant productivity. This general framework should also be useful for plant and animal ecology.

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