Spatial organization of intestinal microbiota in the mouse ascending colon

Nava, Gerardo M.; Friedrichsen, Hans J; Stappenbeck, Thaddeus S.

doi:10.1038/ismej.2010.161

Cited by 233 publications

(202 citation statements)

References 60 publications

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“…In particular, we find that mixtures of rod-shaped and coccal cells can produce layered colony structures, as observed previously in both biotic and abiotic environments (36,45). This result extends our understanding of the functional value of cell shape, both as a competitive phenotype in the biofilm context and as a means for bacteria to influence their environment through collective action.…”

Section: Discussionsupporting

confidence: 69%

Cell morphology drives spatial patterning in microbial communities

Smith

Davit

Osborne

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

156

138

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The clearest phenotypic characteristic of microbial cells is their shape, but we do not understand how cell shape affects the dense communities, known as biofilms, where many microbes live. Here, we use individual-based modeling to systematically vary cell shape and study its impact in simulated communities. We compete cells with different cell morphologies under a range of conditions and ask how shape affects the patterning and evolutionary fitness of cells within a community. Our models predict that cell shape will strongly influence the fate of a cell lineage: we describe a mechanism through which coccal (round) cells rise to the upper surface of a community, leading to a strong spatial structuring that can be critical for fitness. We test our predictions experimentally using strains of Escherichia coli that grow at a similar rate but differ in cell shape due to single amino acid changes in the actin homolog MreB. As predicted by our model, cell types strongly sort by shape, with round cells at the top of the colony and rod cells dominating the basal surface and edges. Our work suggests that cell morphology has a strong impact within microbial communities and may offer new ways to engineer the structure of synthetic communities.biofilms | cell morphology | biophysics | self-organization | synthetic biology S ingle-celled microorganisms such as bacteria display significant morphological diversity, ranging from the simple to the complex and exotic (1-3). Phylogenetic studies indicate that particular morphologies have evolved independently multiple times, suggesting that the myriad shapes of modern bacteria may be adaptations to particular environments (4-6). Microbes can also actively change their morphology in response to environmental stimuli, such as changes to nutrient levels or predation (7,8). However, understanding when and why particular cell shapes offer a competitive edge remains an unresolved question in microbiology.Previous studies have characterized selective pressures favoring particular shapes (7, 9-11): for example, highly viscous environments may select for the helical cell morphologies observed in spirochete bacteria (12). Thus far, these studies have predominantly focused on selective pressures acting at the level of the individual cell. However, many species live in dense, surfaceassociated communities known as biofilms, which are fundamental to the biology of microbes and how they affect us-playing major roles in the human microbiome, chronic diseases, antibiotic resistance, biofouling, and waste-water treatment (13-17). As a result, there has been an intensive effort in recent years to understand how the biofilm mode of growth affects microbes and their evolution (18, 19), but we know very little of the importance of cell shape for biofilm biology.In biofilms, microbial cells are often in close physical contact, making mechanical interactions between neighboring cells particularly significant. Recent studies have suggested that rodshaped cells can drive collective behaviors in microbial g...

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Section: Discussionsupporting

confidence: 69%

Cell morphology drives spatial patterning in microbial communities

Smith

Davit

Osborne

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

156

138

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“…on the mucosa, and an enrichment of Bacteroidaceae, Enterococcaceae and Lactobacillaceae spp. in the lumen (Nava et al, 2011). Despite these reported patterns, other studies have shown significant heterogeneity of mucosal bacterial communities within individuals (Zhang et al, 2014).…”

Section: Introductionmentioning

confidence: 49%

“…increased in both the lumen and mucosa with antibiotics and could represent a beneficial effect of ASP250. Members of this genus are known to produce bacteriocins (antimicrobial compounds) and butyrate, are associated with the colonic mucosa of mice (Nava et al, 2011), and have been considered as a potential direct-fed microbial (that is, probiotic) in livestock production (McAllister et al, 2011). In contrast, a collateral effect of ASP250 was on E. coli, populations of which are known to increase with ASP250 and certain other gut disturbances (Allen et al, 2011;Looft et al, 2012).…”

Section: Gut Microbes Subdivided By Location and Treatment T Looft Et Almentioning

confidence: 84%

Bacteria, phages and pigs: the effects of in-feed antibiotics on the microbiome at different gut locations

Looft

Allen

Cantarel³

et al. 2014

The ISME Journal

330

265

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Disturbance of the beneficial gut microbial community is a potential collateral effect of antibiotics, which have many uses in animal agriculture (disease treatment or prevention and feed efficiency improvement). Understanding antibiotic effects on bacterial communities at different intestinal locations is essential to realize the full benefits and consequences of in-feed antibiotics. In this study, we defined the lumenal and mucosal bacterial communities from the small intestine (ileum) and large intestine (cecum and colon) plus feces, and characterized the effects of in-feed antibiotics (chlortetracycline, sulfamethazine and penicillin (ASP250)) on these communities. 16S rRNA gene sequence and metagenomic analyses of bacterial membership and functions revealed dramatic differences between small and large intestinal locations, including enrichment of Firmicutes and phage-encoding genes in the ileum. The large intestinal microbiota encoded numerous genes to degrade plant cell wall components, and these genes were lacking in the ileum. The mucosaassociated ileal microbiota harbored greater bacterial diversity than the lumen but similar membership to the mucosa of the large intestine, suggesting that most gut microbes can associate with the mucosa and might serve as an inoculum for the lumen. The collateral effects on the microbiota of antibiotic-fed animals caused divergence from that of control animals, with notable changes being increases in Escherichia coli populations in the ileum, Lachnobacterium spp. in all gut locations, and resistance genes to antibiotics not administered. Characterizing the differential metabolic capacities and response to perturbation at distinct intestinal locations will inform strategies to improve gut health and food safety.

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“…Concordant with the fact that this cluster includes many acetate-and/or lactate-converting butyrate producers, the simulation of a mucosal environment induced a shift from acetate towards butyrate, independent of the inoculum. Despite the fact that, in living animals, the continuous desquamation of mucus into the luminal content obscures the distinction between luminal and mucosal microbes, recent in vivo studies also show an enrichment of Firmicutes (especially Clostridium cluster XIVa4 Lachnospiraceae family), over Bacteroidetes in biopsies compared with luminal or faecal samples, both in rodents (Hill et al, 2009;Nava et al, 2011) and humans (Eckburg et al, 2005;Frank et al, 2007;Shen et al, 2010;Wang et al, 2010;Willing et al, 2010;Hong et al, 2011). This in vivo enrichment of Firmicutes in mucus, although sometimes less strong as during our in vitro study, suggests that similar forces may drive the mucosal microbiota composition in vivo and in vitro, likely to include selection of specific groups that adhere to mucins (Leitch et al, 2007) or insoluble substrates in general (Walker et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, by locally excreting antimicrobials or competing with pathogens, mucosal microbes more effectively limit pathogen translocation. Besides host immune effectors (Lievin-Le Moal and Servin, 2006), microbial properties, such as mucus adhesion (Roos and Jonsson, 2002) or the ability to degrade host-derived glycans (Derrien et al, 2004), also impact the distinct surface-attached microbial composition, generally characterized by an enrichment of Firmicutes (especially Clostridium cluster XIVa) over Bacteroidetes (Eckburg et al, 2005;Frank et al, 2007;Hill et al, 2009;Shen et al, 2010;Willing et al, 2010;Hong et al, 2011;Nava et al, 2011). Moreover, the mucus layer is persistently colonized by all types of hydrogenotrophs: methanogenic archaea, sulphate-reducing bacteria and acetogenic bacteria (Nava et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model

et al. 2012

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The human gut is colonized by a complex microbiota with multiple benefits. Although the surfaceattached, mucosal microbiota has a unique composition and potential to influence human health, it remains difficult to study in vivo. Therefore, we performed an in-depth microbial characterization (human intestinal tract chip (HITChip)) of a recently developed dynamic in vitro gut model, which simulates both luminal and mucosal gut microbes (mucosal-simulator of human intestinal microbial ecosystem (M-SHIME)). Inter-individual differences among human subjects were confirmed and microbial patterns unique for each individual were preserved in vitro. Furthermore, in correspondence with in vivo studies, Bacteroidetes and Proteobacteria were enriched in the luminal content while Firmicutes rather colonized the mucin layer, with Clostridium cluster XIVa accounting for almost 60% of the mucin-adhered microbiota. Of the many acetate and/or lactate-converting butyrate producers within this cluster, Roseburia intestinalis and Eubacterium rectale most specifically colonized mucins. These 16S rRNA gene-based results were confirmed at a functional level as butyryl-CoA:acetate-CoA transferase gene sequences belonged to different species in the luminal as opposed to the mucin-adhered microbiota, with Roseburia species governing the mucosal butyrate production. Correspondingly, the simulated mucosal environment induced a shift from acetate towards butyrate. As not only inter-individual differences were preserved but also because compared with conventional models, washout of relevant mucin-adhered microbes was avoided, simulating the mucosal gut microbiota represents a breakthrough in modeling and mechanistically studying the human intestinal microbiome in health and disease. Finally, as mucosal butyrate producers produce butyrate close to the epithelium, they may enhance butyrate bioavailability, which could be useful in treating diseases, such as inflammatory bowel disease.

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Spatial organization of intestinal microbiota in the mouse ascending colon

Cited by 233 publications

References 60 publications

Cell morphology drives spatial patterning in microbial communities

Cell morphology drives spatial patterning in microbial communities

Bacteria, phages and pigs: the effects of in-feed antibiotics on the microbiome at different gut locations

Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model

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