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Article ; Online: Immunogenetic variation shapes the gut microbiome in a natural vertebrate population.

Davies, Charli S / Worsley, Sarah F / Maher, Kathryn H / Komdeur, Jan / Burke, Terry / Dugdale, Hannah L / Richardson, David S

Microbiome

2022 Volume 10, Issue 1, Page(s) 41

Abstract: Background: The gut microbiome (GM) can influence many biological processes in the host, impacting its health and survival, but the GM can also be influenced by the host's traits. In vertebrates, Major Histocompatibility Complex (MHC) genes play a ... ...

Abstract	Background: The gut microbiome (GM) can influence many biological processes in the host, impacting its health and survival, but the GM can also be influenced by the host's traits. In vertebrates, Major Histocompatibility Complex (MHC) genes play a pivotal role in combatting pathogens and are thought to shape the host's GM. Despite this-and the documented importance of both GM and MHC variation to individual fitness-few studies have investigated the association between the GM and MHC in the wild. Results: We characterised MHC class I (MHC-I), MHC class II (MHC-II) and GM variation in individuals within a natural population of the Seychelles warbler (Acrocephalus sechellensis). We determined how the diversity and composition of the GM varied with MHC characteristics, in addition to environmental factors and other host traits. Our results show that the presence of specific MHC alleles, but not MHC diversity, influences both the diversity and composition of the GM in this population. MHC-I alleles, rather than MHC-II alleles, had the greatest impact on the GM. GM diversity was negatively associated with the presence of three MHC-I alleles (Ase-ua3, Ase-ua4, Ase-ua5), and one MHC-II allele (Ase-dab4), while changes in GM composition were associated with the presence of four different MHC-I alleles (Ase-ua1, Ase-ua7, Ase-ua10, Ase-ua11). There were no associations between GM diversity and TLR3 genotype, but GM diversity was positively correlated with genome-wide heterozygosity and varied with host age and field period. Conclusions: These results suggest that components of the host's immune system play a role in shaping the GM of wild animals. Host genotype-specifically MHC-I and to a lesser degree MHC-II variation-can modulate the GM, although whether this occurs directly, or indirectly through effects on host health, is unclear. Importantly, if immune genes can regulate host health through modulation of the microbiome, then it is plausible that the microbiome could also influence selection on immune genes. As such, host-microbiome coevolution may play a role in maintaining functional immunogenetic variation within natural vertebrate populations. Video abstract.
MeSH term(s)	Alleles ; Animals ; Gastrointestinal Microbiome/genetics ; Genetic Variation/genetics ; Immunogenetics ; Selection, Genetic ; Vertebrates/genetics
Language	English
Publishing date	2022-03-08
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Video-Audio Media
ZDB-ID	2697425-3
ISSN	2049-2618 ; 2049-2618
ISSN (online)	2049-2618
ISSN	2049-2618
DOI	10.1186/s40168-022-01233-y
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Efficient assembly and long-term stability of defensive microbiomes via private resources and community bistability.

Boza, Gergely / Worsley, Sarah F / Yu, Douglas W / Scheuring, István

PLoS computational biology

2019 Volume 15, Issue 5, Page(s) e1007109

Abstract: Understanding the mechanisms that promote the assembly and maintenance of host-beneficial microbiomes is an open problem. Empirical evidence supports the idea that animal and plant hosts can combine 'private resources' with the ecological phenomenon ... ...

Abstract	Understanding the mechanisms that promote the assembly and maintenance of host-beneficial microbiomes is an open problem. Empirical evidence supports the idea that animal and plant hosts can combine 'private resources' with the ecological phenomenon known as 'community bistability' to favour some microbial strains over others. We briefly review evidence showing that hosts can: (i) protect the growth of beneficial strains in an isolated habitat, (ii) use antibiotics to suppress non-beneficial, competitor strains, and (iii) provide resources that only beneficial strains are able to translate into an increased rate of growth, reproduction, or antibiotic production. We then demonstrate in a spatially explicit, individual-based model that these three mechanisms act similarly by selectively promoting the initial proliferation of preferred strains, that is, by acting as a private resource. The faster early growth of preferred strains, combined with the phenomenon of 'community bistability,' allows those strains to continue to dominate the microbiome even after the private resource is withdrawn or made public. This is because after a beneficial colony reaches a sufficiently large size, it can resist invasion by parasites without further private support from the host. We further explicitly model localized microbial interactions and diffusion dynamics, and we show that an intermediate level of antibiotic diffusion is the most efficient mechanism in promoting preferred strains and that there is a wide range of parameters under which hosts can promote the assembly of a self-sustaining defensive microbiome. This in turn supports the idea that hosts readily evolve to promote host-beneficial defensive microbiomes.
MeSH term(s)	Animals ; Anti-Bacterial Agents/biosynthesis ; Computational Biology ; Ecosystem ; Host Microbial Interactions/physiology ; Microbiota/physiology ; Models, Biological ; Symbiosis/physiology
Chemical Substances	Anti-Bacterial Agents
Language	English
Publishing date	2019-05-31
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2193340-6
ISSN	1553-7358 ; 1553-734X
ISSN (online)	1553-7358
ISSN	1553-734X
DOI	10.1371/journal.pcbi.1007109
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Article: Biocontrol of Cereal Crop Diseases Using Streptomycetes

Newitt, Jake T / Prudence, Samuel M. M / Hutchings, Matthew I / Worsley, Sarah F

Pathogens. 2019 June 13, v. 8, no. 2

2019

Abstract: A growing world population and an increasing demand for greater food production requires that crop losses caused by pests and diseases are dramatically reduced. Concurrently, sustainability targets mean that alternatives to chemical pesticides are ... ...

Abstract	A growing world population and an increasing demand for greater food production requires that crop losses caused by pests and diseases are dramatically reduced. Concurrently, sustainability targets mean that alternatives to chemical pesticides are becoming increasingly desirable. Bacteria in the plant root microbiome can protect their plant host against pests and pathogenic infection. In particular, Streptomyces species are well-known to produce a range of secondary metabolites that can inhibit the growth of phytopathogens. Streptomyces are abundant in soils and are also enriched in the root microbiomes of many different plant species, including those grown as economically and nutritionally valuable cereal crops. In this review we discuss the potential of Streptomyces to protect against some of the most damaging cereal crop diseases, particularly those caused by fungal pathogens. We also explore factors that may improve the efficacy of these strains as biocontrol agents in situ, as well as the possibility of exploiting plant mechanisms, such as root exudation, that enable the recruitment of microbial species from the soil to the root microbiome. We argue that a greater understanding of these mechanisms may enable the development of protective plant root microbiomes with a greater abundance of beneficial bacteria, such as Streptomyces species.
Keywords	Streptomyces ; bacteria ; beneficial microorganisms ; biological control ; biological control agents ; crop losses ; exudation ; food production ; fungi ; grain crops ; host plants ; microbiome ; pests ; plant pathogens ; roots ; secondary metabolites ; soil
Language	English
Dates of publication	2019-0613
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2695572-6
ISSN	2076-0817
ISSN	2076-0817
DOI	10.3390/pathogens8020078
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Soil, senescence and exudate utilisation: characterisation of the Paragon var. spring bread wheat root microbiome.

Prudence, Samuel Mm / Newitt, Jake T / Worsley, Sarah F / Macey, Michael C / Murrell, J Colin / Lehtovirta-Morley, Laura E / Hutchings, Matthew I

Environmental microbiome

2021 Volume 16, Issue 1, Page(s) 12

Abstract: Background: Conventional methods of agricultural pest control and crop fertilisation are unsustainable. To meet growing demand, we must find ecologically responsible means to control disease and promote crop yields. The root-associated microbiome can ... ...

Abstract	Background: Conventional methods of agricultural pest control and crop fertilisation are unsustainable. To meet growing demand, we must find ecologically responsible means to control disease and promote crop yields. The root-associated microbiome can aid plants with disease suppression, abiotic stress relief, and nutrient bioavailability. The aim of the present work was to profile the community of bacteria, fungi, and archaea associated with the wheat rhizosphere and root endosphere in different conditions. We also aimed to use Results: Metabarcoding revealed that community composition shifted significantly for bacteria, fungi, and archaea across compartments. This shift was most pronounced for bacteria and fungi, while we observed weaker selection on the ammonia oxidising archaea-dominated archaeal community. Across multiple soil types we found that soil inoculum was a significant driver of endosphere community composition, however, several bacterial families were identified as core enriched taxa in all soil conditions. The most abundant of these were Streptomycetaceae and Burkholderiaceae. Moreover, as the plants senesce, both families were reduced in abundance, indicating that input from the living plant was required to maintain their abundance in the endosphere. Stable isotope probing showed that bacterial taxa within the Burkholderiaceae family, among other core enriched taxa such as Pseudomonadaceae, were able to use root exudates, but Streptomycetaceae were not. Conclusions: The consistent enrichment of Streptomycetaceae and Burkholderiaceae within the endosphere, and their reduced abundance after developmental senescence, indicated a significant role for these families within the wheat root microbiome. While Streptomycetaceae did not utilise root exudates in the rhizosphere, we provide evidence that Pseudomonadaceae and Burkholderiaceae family taxa are recruited to the wheat root community via root exudates. This deeper understanding crop microbiome formation will enable researchers to characterise these interactions further, and possibly contribute to ecologically responsible methods for yield improvement and biocontrol in the future.
Language	English
Publishing date	2021-06-21
Publishing country	England
Document type	Journal Article
ISSN	2524-6372
ISSN (online)	2524-6372
DOI	10.1186/s40793-021-00381-2
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Article: Investigating the Role of Root Exudates in Recruiting

Worsley, Sarah F / Macey, Michael C / Prudence, Samuel M M / Wilkinson, Barrie / Murrell, J Colin / Hutchings, Matthew I

Frontiers in molecular biosciences

2021 Volume 8, Page(s) 686110

Abstract: ... ...

Abstract	Streptomyces
Language	English
Publishing date	2021-06-16
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2814330-9
ISSN	2296-889X
ISSN	2296-889X
DOI	10.3389/fmolb.2021.686110
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Article ; Online: Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population.

Worsley, Sarah F / Davies, Charli S / Mannarelli, Maria-Elena / Hutchings, Matthew I / Komdeur, Jan / Burke, Terry / Dugdale, Hannah L / Richardson, David S

Animal microbiome

2021 Volume 3, Issue 1, Page(s) 84

Abstract: Background: The vertebrate gut microbiome (GM) can vary substantially across individuals within the same natural population. Although there is evidence linking the GM to health in captive animals, very little is known about the consequences of GM ... ...

Abstract	Background: The vertebrate gut microbiome (GM) can vary substantially across individuals within the same natural population. Although there is evidence linking the GM to health in captive animals, very little is known about the consequences of GM variation for host fitness in the wild. Here, we explore the relationship between faecal microbiome diversity, body condition, and survival using data from the long-term study of a discrete natural population of the Seychelles warbler (Acrocephalus sechellensis) on Cousin Island. To our knowledge, this is the first time that GM differences associated with survival have been fully characterised for a natural vertebrate species, across multiple age groups and breeding seasons. Results: We identified substantial variation in GM community structure among sampled individuals, which was partially explained by breeding season (5% of the variance), and host age class (up to 1% of the variance). We also identified significant differences in GM community membership between adult birds that survived, versus those that had died by the following breeding season. Individuals that died carried increased abundances of taxa that are known to be opportunistic pathogens, including several ASVs in the genus Mycobacterium. However, there was no association between GM alpha diversity (the diversity of bacterial taxa within a sample) and survival to the next breeding season, or with individual body condition. Additionally, we found no association between GM community membership and individual body condition. Conclusions: These results demonstrate that components of the vertebrate GM can be associated with host fitness in the wild. However, further research is needed to establish whether changes in bacterial abundance contribute to, or are only correlated with, differential survival; this will add to our understanding of the importance of the GM in the evolution of host species living in natural populations.
Language	English
Publishing date	2021-12-20
Publishing country	England
Document type	Journal Article
ISSN	2524-4671
ISSN (online)	2524-4671
DOI	10.1186/s42523-021-00149-6
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Article: Biocontrol of Cereal Crop Diseases Using Streptomycetes.

Newitt, Jake T / Prudence, Samuel M M / Hutchings, Matthew I / Worsley, Sarah F

Pathogens (Basel, Switzerland)

2019 Volume 8, Issue 2

Abstract	A growing world population and an increasing demand for greater food production requires that crop losses caused by pests and diseases are dramatically reduced. Concurrently, sustainability targets mean that alternatives to chemical pesticides are becoming increasingly desirable. Bacteria in the plant root microbiome can protect their plant host against pests and pathogenic infection. In particular,
Language	English
Publishing date	2019-06-13
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2695572-6
ISSN	2076-0817
ISSN	2076-0817
DOI	10.3390/pathogens8020078
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Article ; Online: Characterisation of the symbionts in the Mediterranean fruit fly gut.

Darrington, Mike / Leftwich, Philip T / Holmes, Neil A / Friend, Lucy A / Clarke, Naomi V E / Worsley, Sarah F / Margaritopolous, John T / Hogenhout, Saskia A / Hutchings, Matthew I / Chapman, Tracey

Microbial genomics

2022 Volume 8, Issue 4

Abstract: Symbioses between bacteria and their insect hosts can range from loose associations through to obligate interdependence. While fundamental evolutionary insights have been gained from the in-depth study of obligate mutualisms, there is increasing interest ...

Abstract	Symbioses between bacteria and their insect hosts can range from loose associations through to obligate interdependence. While fundamental evolutionary insights have been gained from the in-depth study of obligate mutualisms, there is increasing interest in the evolutionary potential of flexible symbiotic associations between hosts and their gut microbiomes. Understanding relationships between microbes and hosts also offers the potential for exploitation for insect control. Here, we investigate the gut microbiome of a global agricultural pest, the Mediterranean fruit fly (
MeSH term(s)	Animals ; Bacteria ; Ceratitis capitata/genetics ; Ceratitis capitata/microbiology ; Klebsiella/genetics ; Phylogeny ; RNA, Ribosomal, 16S/genetics ; Symbiosis
Chemical Substances	RNA, Ribosomal, 16S
Language	English
Publishing date	2022-04-21
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2835258-0
ISSN	2057-5858 ; 2057-5858
ISSN (online)	2057-5858
ISSN	2057-5858
DOI	10.1099/mgen.0.000801
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Article ; Online: Streptomyces

Worsley, Sarah F / Newitt, Jake / Rassbach, Johannes / Batey, Sibyl F D / Holmes, Neil A / Murrell, J Colin / Wilkinson, Barrie / Hutchings, Matthew I

Applied and environmental microbiology

2020 Volume 86, Issue 16

Abstract: ... ...

Abstract	Streptomyces
MeSH term(s)	Arabidopsis/growth & development ; Arabidopsis/microbiology ; Arabidopsis/physiology ; Endophytes/physiology ; Host Microbial Interactions ; Seedlings/growth & development ; Seedlings/microbiology ; Soil Microbiology ; Streptomyces/physiology ; Triticum/growth & development ; Triticum/microbiology ; Triticum/physiology
Language	English
Publishing date	2020-08-03
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	223011-2
ISSN	1098-5336 ; 0099-2240
ISSN (online)	1098-5336
ISSN	0099-2240
DOI	10.1128/AEM.01053-20
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Article ; Online: Chemical ecology of antibiotic production by actinomycetes.

van der Meij, Anne / Worsley, Sarah F / Hutchings, Matthew I / van Wezel, Gilles P

FEMS microbiology reviews

2017 Volume 41, Issue 3, Page(s) 392–416

Abstract: Actinomycetes are a diverse family of filamentous bacteria that produce a plethora of natural products relevant for agriculture, biotechnology and medicine, including the majority of the antibiotics we use in the clinic. Rather than as free-living ... ...

Abstract	Actinomycetes are a diverse family of filamentous bacteria that produce a plethora of natural products relevant for agriculture, biotechnology and medicine, including the majority of the antibiotics we use in the clinic. Rather than as free-living bacteria, many actinomycetes have evolved to live in symbiosis with among others plants, fungi, insects and sponges. As a common theme, these organisms profit from the natural products and enzymes produced by the actinomycetes, for example, for protection against pathogenic microbes, for growth promotion or for the degradation of complex natural polymers such as lignocellulose. At the same time, the actinomycetes benefit from the resources of the hosts they interact with. Evidence is accumulating that these interactions control the expression of biosynthetic gene clusters and have played a major role in the evolution of the high chemical diversity of actinomycete-produced secondary metabolites. Many of the biosynthetic gene clusters for antibiotics are poorly expressed under laboratory conditions, but they are likely expressed in response to host-specific demands. Here, we review the environmental triggers and cues that control natural product formation by actinomycetes and provide pointers as to how these insights may be harnessed for drug discovery.
Language	English
Publishing date	2017-05-01
Publishing country	England
Document type	Journal Article
ZDB-ID	283740-7
ISSN	1574-6976 ; 0168-6445
ISSN (online)	1574-6976
ISSN	0168-6445
DOI	10.1093/femsre/fux005
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