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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

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
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


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

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
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


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