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Microbiome: A Joint Virtual Issue from the BSI and the Microbiology Society

Gut microbe

To celebrate World Microbiome Day 2018 on 27th June, the British Society for Immunology and the Microbiology Society are pleased to present a joint Virtual Issue on the microbiome.

Immunology and Clinical & Experimental Immunology have long been at the forefront of journals offering a platform to immunologists seeking to narrate the exciting, evolving narrative of the interplay between microbiota-health or dysbiosis, immune subsets, inflammation and disease. The papers assembled for this collection offer a state-of-the art appraisal from many of the leading immunologists who have been working in this area. The wide array of pathologies discussed in this set – from autoimmune and inflammatory disease to bacterial sepsis, parasitic infection and obesity – offer a window onto the importance of microbiota for shaping the immune programme.

The aim of this set has been to offer a tour through current trends and passions in the field. Papers on Prevotella, segmented filamentous bacteria and other microbiota species set the scene, reminding us that immunologists still have much work ahead in defining the rules of how our thousand-plus passengers interact with immune receptors. Part of the new toolbox that has had to develop alongside this is the analysis of bacterial metabolites and their impacts on immune and inflammatory function.

Several studies in this collection describe detailed aspects of the interaction between diet, microbiota, immune subset differentiation, bacterial metabolites and disease. This will be a really important area to populate (funders – please take note!), with potentially enormous rewards. Immunology’s many outstanding contributions to modern biomedicine, including monoclonal antibody therapies, cancer checkpoint blockade and CAR T cells, have shared the property of being very challenging to healthcare economics. The promised revolution from greater understanding and manipulation of the microbiota-immune system axis offers the potential for our next great contribution, with many of the solutions affordable and accessible.   

Alongside a jointly-published editorial by Professor Julian Marchesi outlining the need for greater collaboration between all subdisciplines in the field of microbiome research, we present articles from across the Societies’ collections and a video from the Editor-in-Chief of Immunology, Professor Daniel Altmann.

All articles in this collection are free to view online.


Joint Editorial from the BSI and MS

 Advancing Microbiology Research

Julian R. Marchesi

Immunology, 2018. doi:10.1111/imm.12973


From the BSI



Segmented filamentous bacteria‐induced immune responses: a balancing act between host protection and autoimmunity

Kyle L. Flannigan, Timothy L. Denning

Immunology, 2018. doi:10.1111/imm.12950


Impacts of microbiome metabolites on immune regulation and autoimmunity

Stefanie Haase, Aiden Haghikia, Nicola Wilck, Dominik N Müller, Ralf A Linker

Immunology, 2018. 154: 230-238. doi:10.1111/imm.12933


The role of salt for immune cell function and disease

Ralf Willebrand, Markus Kleinewietfeld

Immunology, 2018. 154: 346-353. doi:10.1111/imm.12915


Adaptive immune education by gut microbiota antigens

Qing Zhao, Charles O. Elson

Immunology, 2018. 154: 28-37. doi:10.1111/imm.12896


Harnessing the power of regulatory T‐cells to control autoimmune diabetes: overview and perspective

Hua Yu, Ricardo Paiva, Richard A. Flavell

Immunology, 2017. 153: 161-170. doi:10.1111/imm.12867


Intestinal dysbiosis and probiotic applications in autoimmune diseases (2017)

Gislane Lelis Vilela de Oliveira, Aline Zazeri Leite, Bruna Stevanato Higuchi, Marina Ignácio Gonzaga, Vânia Sammartino Mariano

Immunology, 2017. 152: 1-12. doi:10.1111/imm.12765


Inflammation and Inflammatory Disease

Interleukin‐23 promotes intestinal T helper type17 immunity and ameliorates obesity‐associated metabolic syndrome in a murine high‐fat diet model (2018)

Larissa M. S. Martins, Malena M. Perez, Camila A. Pereira, Frederico R. C. Costa, Murilo S. Dias, Rita C. Tostes, Simone G. Ramos, Marcel R. de Zoete, Bernhard Ryffel, João S. Silva, Daniela Carlos

Immunology, 2018. doi:10.1111/imm.12946


Inflammatory bowel disease and immunonutrition: novel therapeutic approaches through modulation of diet and the gut microbiome

Larissa S. Celiberto, Franziska A. Graef, Genelle R. Healey, Else S. Bosman, Kevan Jacobson, Laura M. Sly, Bruce A. Vallance

Immunology, 2018. doi:10.1111/imm.12939


Immune regulation by microbiome metabolites

Chang H. Kim

Immunology, 2018. 154: 220-229. doi:10.1111/imm.12930


Inflammation in CNS Neurodegenerative Diseases

Jodie Stephenson, Erik Nutma, Paul van der Valk, Sandra Amor

Immunology, 2018. 154: 204-219. doi:10.1111/imm.12922


The role of gut microbiome and associated metabolome in the regulation of neuroinflammation in multiple sclerosis and its implications in attenuating chronic inflammation in other inflammatory and autoimmune disorders

Nicholas Dopkins, Prakash S. Nagarkatti, Mitzi Nagarkatti

Immunology, 2018. 154: 178-185. doi:10.1111/imm.12903


The immune response to Prevotella bacteria in chronic inflammatory disease

Jeppe Madura Larsen

Immunology, 2017. 151: 363-374. doi:10.1111/imm.12760


Intestinal colonization resistance

Trevor D. Lawley, Alan W. Walker

Immunology, 2012. 138: 1-11. doi:10.1111/j.1365-2567.2012.03616.x


Immune regulation

The mechanisms shaping the repertoire of CD4+ Foxp3+ regulatory T cells

Piotr Kraj, Leszek Ignatowicz

Immunology, 2017. 153: 290-296. doi:10.1111/imm.12859


Immune surveillance

Communicating systems in the body: how microbiota and microglia cooperate

Daniel Erny, Anna Lena Hrabě de Angelis, Marco Prinz

Immunology, 2016. 150: 7-15. doi:10.1111/imm.12645


Clinical & Experimental Immunology

Immune Regulation

Differential responses of human dendritic cells to metabolites from the oral/airway microbiome

K. Whiteson, S. Agrawal, A. Agrawal

Clin Exp Immunol, 2017. 188: 371-379. doi:10.1111/cei.12943


Infection and Infectious Disease

Lack of host gut microbiota alters immune responses and intestinal granuloma formation during schistosomiasis

M. Holzscheiter, L. E. Layland, E. Loffredo‐Verde, K. Mair, R. Vogelmann, R. Langer, H. Wagner, C. Prazeres da Costa

Clin Exp Immunol, 2013. 175: 246-257. doi:10.1111/cei.12230


Immune mechanisms and the impact of the disrupted lung microbiome in chronic bacterial lung infection and bronchiectasis

R. J. Boyton, C. J. Reynolds, K. J. Quigley, D. M. Altmann

Clin Exp Immunol, 2012. 171: 117-123. doi:10.1111/cei.12003


Inflammation and Inflammatory Disease

C4B gene influences intestinal microbiota through complement activation in patients with paediatric‐onset inflammatory bowel disease

E. Nissilä, K. Korpela, A. I. Lokki, R. Paakkanen, S. Jokiranta, W. M. de Vos, M.‐L. Lokki, K.‐L. Kolho S. Meri

Clin Exp Immunol, 2017. 190: 394-405. doi:10.1111/cei.13040


Proinflammatory cytokine interferon‐γ and microbiome‐derived metabolites dictate epigenetic switch between forkhead box protein 3 isoforms in coeliac disease

G. Serena, S. Yan, S. Camhi, S. Patel, R. S. Lima, A. Sapone, M. M. Leonard, R. Mukherjee, B. J. Nath, K. M. Lammers, A. Fasano

Clin Exp Immunol, 2017. 187: 490-506. doi:10.1111/cei.12911

Gut microbiome in children with enthesitis‐related arthritis in a developing country and the effect of probiotic administration

A. Aggarwal, A. N. Sarangi, P. Gaur, A. Shukla, R. Aggarwal

Clin Exp Immunol, 2016. 187: 480-489. doi:10.1111/cei.12900


The immunology of the vermiform appendix: a review of the literature

I. A. Kooij, S. Sahami, S. L. Meijer, C. J. Buskens, A. A. te Velde

Clin Exp Immunol, 2016. 186: 1-9. doi:10.1111/cei.12821


Free and complexed‐secretory immunoglobulin A triggers distinct intestinal epithelial cell responses

R. Salerno‐Goncalves, F. Safavie, A. Fasano, M. B. Sztein

Clin Exp Immunol, 2016. 185: 338-347. doi:10.1111/cei.12801


Impact of dietary deviation on disease progression and gut microbiome composition in lupus‐prone SNF1 mice  

B. M. Johnson, M.‐C. Gaudreau, M. M. Al‐Gadban, R. Gudi, C. Vasu

Clin Exp Immunol, 2015. 181: 323-337. doi:10.1111/cei.12609


Immune homeostasis, dysbiosis and therapeutic modulation of the gut microbiota

C. T. Peterson, V. Sharma, L. Elmén, S. N. Peterson

Clin Exp Immunol, 2014. 179: 363-377. doi:10.1111/cei.12474


From the Review Series ‘Focus on Hygiene Hypothesis and Approaches to Modulating the Microbiome

The intestinal microbiome in type 1 diabetes

J. L. Dunne, E. W. Triplett, D. Gevers, R. Xavier, R. Insel, J. Danska, M. A. Atkinson

Clin Exp Immunol, 2014. 177: 30-37. doi:10.1111/cei.12321


Intestinal microbiota and faecal transplantation as treatment modality for insulin resistance and type 2 diabetes mellitus

S. D. Udayappan, A. V. Hartstra, G. M. Dallinga‐Thie, M. Nieuwdorp

Clin Exp Immunol, 2014. 177: 24-29. doi:10.1111/cei.12293


Microbial ‘old friends’, immunoregulation and socioeconomic status

G. A. W. Rook, C. L. Raison, C. A. Lowry

Clin Exp Immunol, 2014. 177: 1-12. doi:10.1111/cei.12269


Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD)

R. Duchmann, I. Kaiser, E. Hermann, W. Mayet, K. Ewe, K.-H. Meyer Zum Büschenfelde

Clin Exp Immunol, 1995. 102: 448-455. doi:10.1111/j.1365-2249.1995.tb03836.x


From the Microbiology Society

Microbial Genomics

Vibrio cholerae genomic diversity within and between patients

Levade I, Terrat Y, Leducq JB, Weil AA, Mayo-Smith LM, Chowdhury F, Khan AI, Boncy J, Buteau J, Ivers LC, Ryan ET, Charles RC, Calderwood SB, Qadri F, Harris JB, LaRocque RC, Shapiro BJ.

Microb Genom. 2017 Dec;3(12). Doi: 10.1099/mgen.0.000142


Novel large-scale chromosomal transfer in Bacteroides fragilis contributes to its pan-genome and rapid environmental adaptation

Husain F, Tang K, Veeranagouda Y, Boente R, Patrick S, Blakely G, Wexler HM.

Microb Genom. 2017 Nov;3(11). doi: 10.1099/mgen.0.000136


Human genome-microbiome interaction: metagenomics frontiers for the aetiopathology of autoimmune diseases

Gundogdu A, Nalbantoglu U.

Microb Genom. 2017 Apr 26;3(4):e000112. doi: 10.1099/mgen.0.000112


Sequence-based analysis of the genus Ruminococcus resolves its phylogeny and reveals strong host association

La Reau AJ, Meier-Kolthoff JP, Suen G.

Microb Genom. 2016 Dec 12;2(12):e000099. doi: 10.1099/mgen.0.000099


First insight into the faecal microbiota of the high Arctic muskoxen (Ovibos moschatus)

Salgado-Flores A, Bockwoldt M, Hagen LH, Pope PB, Sundset MA.

Microb Genom. 2016 Jul 29;2(7):e000066. doi: 10.1099/mgen.0.000066


Polysaccharide utilization loci and nutritional specialization in a dominant group of butyrate-producing human colonic Firmicutes

Sheridan PO, Martin JC, Lawley TD, Browne HP, Harris HM, Bernalier-Donadille A, Duncan SH, O'Toole PW, Scott KP, Flint HJ.

Microb Genom. 2016 Feb 9;2(2):e000043. doi: 10.1099/mgen.0.000043



Impact of stress on the gut microbiome of free-ranging western lowland gorillas

Klára Vlčková, Kathryn Shutt-Phillips, Michael Heistermann, Barbora Pafčo, Klára J. Petrželková, Angelique Todd, David Modrý, Karen E. Nelson, Brenda A. Wilson, Rebecca M. Stumpf, Bryan A. White, Steven R. Leigh, Andres Gomez

January 2018, Microbiology 164: 40-44, doi: 10.1099/mic.0.000587


The soil microbiome at the Gi-FACE experiment responds to a moisture gradient but not to CO2 enrichment

Alexandre B. de Menezes, Christoph Müller, Nicholas Clipson, Evelyn Doyle

September 2016, Microbiology 162: 1572-1582, doi: 10.1099/mic.0.000341


Comparison of Lactobacillus crispatus isolates from Lactobacillus-dominated vaginal microbiomes with isolates from microbiomes containing bacterial vaginosis-associated bacteria

Abdallah A. Abdelmaksoud, Vishal N. Koparde, Nihar U. Sheth, Myrna G. Serrano, Abigail L. Glascock, Jennifer M. Fettweis, Jerome F. Strauss III, Gregory A. Buck, Kimberly K. Jefferson

March 2016, Microbiology 162: 466-475, doi: 10.1099/mic.0.000238


Non-pathogenic Neisseria: members of an abundant, multi-habitat, diverse genus

Guangyu Liu, Christoph M. Tang, Rachel M. Exley

July 2015, Microbiology 161: 1297-1312, doi: 10.1099/mic.0.000086


Differences in vaginal microbiome in African American women versus women of European ancestry

Jennifer M. Fettweis, J. Paul Brooks, Myrna G. Serrano, Nihar U. Sheth, Philippe H. Girerd, David J. Edwards, Jerome F. Strauss III, the Vaginal Microbiome Consortium, Kimberly K. Jefferson, Gregory A. Buck

October 2014, Microbiology 160: 2272-2282, doi: 10.1099/mic.0.081034-0


Bacterial multispecies studies and microbiome analysis of a plant disease

Daniel Passos da Silva, Maria Pilar Castañeda-Ojeda, Chiaraluce Moretti, Roberto Buonaurio, Cayo Ramos, Vittorio Venturi

March 2014, Microbiology 160: 556-566, doi: 10.1099/mic.0.074468-0


An observational study of the microbiome of the maternal pouch and saliva of the tammar wallaby, Macropus eugenii, and of the gastrointestinal tract of the pouch young

Kim-Ly Chhour, Lyn A. Hinds, Nicholas A. Jacques, Elizabeth M. Deane

March 2010, Microbiology 156: 798-808, doi: 10.1099/mic.0.031997-0


The microbiome of the cloacal openings of the urogenital and anal tracts of the tammar wallaby, Macropus eugenii

Kim-Ly Chhour, Lyn A. Hinds, Elizabeth M. Deane, Nicholas A. Jacques

May 2008, Microbiology 154: 1535-1543, doi: 10.1099/mic.0.2007/014803-0


Journal of Medical Microbiology

Short- and long-term influence of the levonorgestrel-releasing intrauterine system (Mirena®) on vaginal microbiota and Candida

Gilbert Gerard Ghislain Donders, G. Bellen, Kateryna Ruban, Ben Van Bulck

March 2018, Journal of Medical Microbiology 67: 308-313, doi: 10.1099/jmm.0.000657


The nursing home elder microbiome stability and associations with age, frailty, nutrition and physical location

John P. Haran, Vanni Bucci, Protiva Dutta, Doyle Ward, Beth McCormick

January 2018, Journal of Medical Microbiology 67: 40-51, doi: 10.1099/jmm.0.000640


The oral microbiome in human immunodeficiency virus (HIV)-positive individuals

James O. Kistler, Pratanporn Arirachakaran, Yong Poovorawan, Gunnar Dahlén, William G. Wade

September 2015, Journal of Medical Microbiology 64: 1094-1101, doi: 10.1099/jmm.0.000128


Are bronchoalveolar lavages a good source for microbial profiling? Differences between throat and bronchoalveolar lavage microbiomes

Alexandra Zimmermann, Gernot Zissel, Joachim Müller-Quernheim, Sylvia Hofmann, Stefan Schreiber, Annegret Fischer

August 2015, Journal of Medical Microbiology 64: 948-951, doi: 10.1099/jmm.0.000112


Probiotics or antibiotics: future challenges in medicine

Yousef Nami, Babak Haghshenas, Norhafizah Abdullah, Abolfazl Barzegari, Dayang Radiah, Rozita Rosli, Ahmad Yari Khosroushahi

February 2015, Journal of Medical Microbiology 64: 137-146, doi: 10.1099/jmm.0.078923-0


Comparative analysis of microbiome between accurately identified 16S rDNA and quantified bacteria in simulated samples

Haiyin Wang, Pengcheng Du, Juan Li, Yuanyuan Zhang, Wen Zhang, Na Han, Patrick C. Y. Woo, Chen Chen

March 2014, Journal of Medical Microbiology 63: 433-440, doi: 10.1099/jmm.0.060616-0


Journal of General Virology

Early nasopharyngeal microbial signature associated with severe influenza in children: a retrospective pilot study

Stanley Langevin, Maxime Pichon, Elise Smith, Juliet Morrison, Zachary Bent, Richard Green, Kristi Barker, Owen Solberg, Yves Gillet, Etienne Javouhey, Bruno Lina, Michael G. Katze, Laurence Josset

October 2017, Journal of General Virology 98: 2425-2437, doi: 10.1099/jgv.0.000920


Viral–bacterial interactions in the respiratory tract

Carla Bellinghausen, Gernot G. U. Rohde, Paul H. M. Savelkoul, Emiel F. M. Wouters, Frank R. M. Stassen

December 2016, Journal of General Virology 97: 3089-3102, doi: 10.1099/jgv.0.000627