Microbiology Today October 2022: Protists

Showcasing the importance of protistology research and engagement activities in collaboration with Protistology-UK.

MICROBIOLOGY TODAY 49:2 October 2022

Protists Showcasing the importance of protistology research and engagement activities in collaboration with Protistology-UK.

Editorial

Welcome to the October 2022 issue of Microbiology Today . I’m writing this editorial on the back of a heatwave (and imminent hosepipe ban) in August – hopefully when you are reading this, we have some cooler and wetter weather coming our way!

I n this issue, I am delighted to showcase articles contributed by members of Protistology-UK, a society which has been affiliated with the Microbiology Society since 2018. It has been a pleasure to work with members of the Protistology-UK elected committee to provide you with this fascinating snapshot of research and engagement activities carried out by their members, and hopefully you will have an equally enjoyable experience as you make your way through the issue. To give you some more details on the theme of this issue, I will pass you on to Fiona Henriquez, Sonja Rueckert, and Anastasios Tsaousis, committee members of Protistology-UK (page 68). For the remainder of my Editorial, I want to highlight some exciting news relating to Microbiology Today . I am very pleased to announce that we are looking for a Deputy Editor of Microbiology Today ! In this role you will work with me for a year to learn about the editorial process before taking over as Editor and Chair of the Editorial Board in 2024. Editor of Microbiology Today has been a great experience for me – not only do you get to hear about the diversity of work being carried out by members of the

Society, but you also get to work with the wonderful and incredibly talented staff at Microbiology Society HQ! If you like the sound of translating the enthusiasm of Society members into print articles, then I urge you to put in an application. Find the full job description and learn how to apply online ( microb.io/jobs ). Applications close on 1 November . If you do have any questions about the role, you are more than welcome to contact me directly. The Editorial Board and Society staff have been working over the past year to define how Microbiology Today can best represent the work and interests of all Society members in 2023 and beyond, and we are very keen to hear from you. I am always delighted to be contacted directly with your thoughts, feedback and suggestions for what you would like to see in future issues of Microbiology Today .

Chris Randall Editor

c.p.randall@leeds.ac.uk @randall_uk

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Contents 49:2 October 2022

Articles

Features

The trojan horse relationship between amoebae and bacteria Ronnie Mooney, Elisa Giammarini, Jackie Parry and Fiona L. Henriquez Exploring how microbial relationships drive antimicrobial resistance. Protists galore for engaging the public James Weiss and Genoveva F. Esteban Revealing the hidden microbial world to the public to improve protistology engagement. Love knows no oxic–anoxic boundaries: anaerobiosis in ciliates provides rich opportunities for microbial symbiosis William H. Lewis and Ross F. Waller A look at anaerobic ciliates and their offering to microbial symbiosis. Gregarine apicomplexans – model organisms to uncover the evolutionary path to obligate intracellular parasitism? Kevin McKinley, Emma Betts, Anastasios D. Tsaousis and Sonja Rueckert Using Gregarine apicomplexans as a tool to understand the evolution of parasitism. Coevolution in the termite–protist symbiosis Gillian H. Gile Insight into the specific relationship protists have with termites allowing them to evolve in parallel with their host. The genetics of prominent plant symbionts: the arbuscular mycorrhizal fungi Nicolas Corradi Microbial genomics and evolution of arbuscular mycorrhizal fungi.

Protists on the spot: opening the field of view on protistology Members of Protistology-UK introduce the importance of protistology.

Microbiology goes Open Access Gavin Thomas writes about the future of our flagship journal, Microbiology .

104

Spotlight on Grants: Education and Outreach Grant A look at Ruth MacLaren’s engagement project, Invisible Worlds, funded by one of our grants. ECM Forum update: reuniting ECMs Rebecca McHugh writes about the first in-person flagship ECM Summer Conference meeting in over two years. Unlocking the potential of our members We’re pleased to announce the first cohort of recipients of the Unlocking Potential Grant.

105

106

107

Member Q&A Meet Vijay Kothari from the Institute of Science, Nirma University, India.

Regulars 61 Editorial

News Updates on Microbiology Society activities.

Introduction to the issue from Chris Randall, Editor of Microbiology Today .

100

Annual Conference Updates on Annual Conference 2023.

Council 2022 The members of Council responsible for governance.

102

Microbiology Society Events and Focused Meetings Details of the 2022 Events and Focused Meeting series.

From the President Gurdyal Besra, President of the Microbiology Society.

108

Reviews The latest book reviews in brief.

From the Chief Executive Peter Cotgreave, Chief Executive of the Microbiology Society.

Chris Randall

Rob King, Kimberley Ndungu Ian Atherton (corbiculadesign.co.uk)

Editor

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Address

Council 2022

Executive Officers

President Professor Gurdyal Besra

General Secretary Professor Mark Harris Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK m.harris@leeds.ac.uk

Treasurer Professor Robin May

School of Biosciences, The University of Birmingham, Edgbaston, Birmingham B15 2TT, UK president@microbiologysociety.org

School of Biosciences and Institute of Microbiology & Infection, The University of Birmingham, Birmingham B15 2TT, UK r.c.may@bham.ac.uk

Co-Chairs and Chairs of Committees Co-Chairs of Sustainability Committee Professor Jose Bengoechea School of Medicine, Dentistry and Biomedical Sciences, 97 Lisburn Road, Belfast BT9 7BL, UK j.bengoechea@qub.ac.uk

Dr Sarah Maddocks Cardiff School of Sport & Health Sciences, Cardiff Metropolitan University, Cardiff CF5 2YB, UK smaddocks@cardiffmet.ac.uk Professor Gill Elliot Department of Microbial Sciences, University of Surrey, Guildford GU2 7XH, UK g.elliott@surrey.ac.uk Dr Tina Joshi School of Biomedical Sciences, University of Plymouth, Portland Square, Plymouth PL4 8AA, UK tina.joshi@plymouth.ac.uk

Professor Paul Hoskisson Strathclyde Institute of Pharmacy and Biomedical Sciences, 161 Cathedral St, Glasgow G4 0RE, UK paul.hoskisson@strath.ac.uk Dr Chloe James School of Science, Engineering and Environment, University of Salford, The Crescent, Salford M5 4WT, UK c.james@salford.ac.uk Colman O’Cathail EMBL-EBI, Wellcome Genome Campus, Hinxton, Cambridgeshire CB10 1SD, UK colman.o-cathail@ucdconnect.ie

Co-Chairs of Building Communities Committee Co-Chairs of Impact and Influence Committee

Chair of Early Career

Microbiologists’ Forum Executive Committee

Elected Members

Professor Laura Bowater

Dr Sharon Brookes Virology Department, Animal and Plant Health Agency, New Haw, Addlestone KT15 3NB, UK sharon.brookes@ apha.gov.uk

Professor Nigel Brown The Microbiology Society, 14-16 Meredith Street, London EC1R 0AB, UK

Dr David Clarke School of Microbiology, University College Cork, Ireland

Dr Andrew Edwards Department of Infectious Disease, Imperial College London, St Mary’s Hospital, Praed Street, London W2 1NY, UK a.edwards@imperial.ac.uk

Professor Kim Hardie Biodiscovery Institute, School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK kim.hardie@ nottingham.ac.uk

University of East Anglia, Norwich Research Park, Norwich, Norfolk NR4 7TJ, UK

laura.bowater@uea.ac.uk

nigel.brown@ed.ac.uk

d.clarke@ucc.ie

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From the President

Welcome to the October issue of Microbiology Today . I want to start by thanking the members of Protistology-UK ( protistology.org.uk ) who have been heavily involved in the production of this issue. This Learned Society (formerly the British Society for Protist Biology) is a membership organisation for scientists and amateurs interested in all areas of protistology, from ecological to medical and from sub-cellular to population studies.

T he Society primarily exists to support and promote protistan research and teaching in the UK, but a key aim is to encourage the development of young scientists. The organisation hosts two scientific meetings a year and provides bursaries for student attendance together with prizes for student presentations. Membership of Protistology-UK is a benefit of Microbiology Society membership – just head to the ‘Update details’ section when you log in and select ‘I would like to be a member of Protistology UK’ under the ‘Get involved’ tab. This is the second Microbiology Today issue of 2022 and my second issue as President of the Microbiology Society. As we come to the final months of the year, I would like to thank all the members who have participated in Society activities and attended events during 2022 – it has been a great pleasure to meet so many of you in my first year as President, and I look forward to opportunities still to come. At our Annual General Meeting in September, we launched the Society’s ambitious new strategy, which lays out our vision, mission and values and will guide our work. In the five years between 2023 and 2027, the Society’s principal goal is to strengthen our culture of being a community-driven Society by amplifying our members’ voices, wherever they are in the world, and empowering them to embed the benefits of microbiology within wider society. The period of the strategy will undoubtedly bring new opportunities and great change for the Society. We will gain a better understanding of the diversity of our members; we will harness local knowledge for worldwide impact; and we will recognise global differences in accessing opportunities. To achieve our ambition, we rely on your ongoing support. In January, our founding journal, Microbiology

( mic.microbiologyresearch.org ), will transition to fully Open Access, the first of the journals in our portfolio to do so. We are doing this because of the benefits Open Access brings to our membership, all microbiologists and those with an interest in microbiology. The world is entering a new era of open science, challenging the status quo by recognising the value of greater transparency and focusing on reproducibility, data management, collaboration and good scientific citizenship. At the Microbiology Society, we embrace these changes and recognise the positive impact they represent for our community, for the scientific endeavour and for society’s understanding of pressing global challenges. We cannot achieve this major change without your support; if you publish one article with us you are benefiting your community. Ask your institution to sign up to our Publish and Read model to give your work a chance to really make a difference – when you publish Open Access with us, your articles will have a greater reach and impact. You can read more about Publish and Read on our journal platform ( microbiologyresearch.org/ publish-and-read ). As always, we are incredibly grateful to all the members who submit to our journals and to those who give up their time to so enthusiastically get involved in everything we do, by joining Committees, Divisions, Panels, Working Groups and by becoming Champions. Thank you all, and I look forward to meeting and hearing from more of you during the remainder of the year and in 2023.

Gurdyal Besra President

president@microbiologysociety.org

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From the Chief Executive

At the Annual General Meeting in September, the President launched the Microbiology Society’s new strategy, which will run from 2023 to 2027. It is the result of months of work by Council members and staff, consultations with various groups of members and assessments of the changing external environment. It would be easy to imagine that all this effort would lead to substantial changes in the strategy, but in the end much of it is unaltered. The changes are focused and important.

A s Council members listened to the membership and thought about how the Microbiology Society can have an even greater impact in the future, they honed in on three things that they want to strengthen. The first is to be ever more inclusive – our values say that we are welcoming to anyone interested in microbes, and the more we can make that a reality, the stronger we will be. Through a better understanding of you, the members, we can better unlock the potential of your broad and deep specialised knowledge. The second emphasis is on the international dimension of the Society’s work. If the last two years have shown us anything, it is that microbes don’t respect national boundaries. What the Microbiology Society seeks to do is harness local knowledge, whichever part of the world it comes from, and use it for worldwide impact. Third, recognising that our strength comes from our membership, Council wants to redouble our efforts to engage with you and to make it easier and ever more rewarding for you to interact with staff and with members of Committees and Editorial Boards so that we can optimise what we do to support and advance your careers in microbiology. The things that remain the same in the strategy are the things that have been unchanging since the wisdom of our founders originally set out the purpose of the Microbiology Society. Our first President, Sir Alexander Fleming, spoke at the inaugural meeting about “bringing together workers in the various branches of microbiology who might not otherwise meet and who would thus get acquainted and talking together – it is in this way that real advances will be made.” Marjory Stephenson, who was offered the founding Presidency before Fleming but modestly turned it down, said “we should make the scope of the Society as wide as possible.” They knew that one of the most crucial ways to advance the science of microbiology was to bring together microbiologists and get

them interacting. The world is now very different – technology, travel, funding, social pressures, the list of changes is endless – but the basic principle has been constant throughout. As we move into the period of the new strategy, one of the most important changes we face is the world of scientific publishing. It is a more competitive, more time-consuming business than it has ever been, and its importance in the lives of researchers has grown relentlessly, as scientists are measured, rewarded and judged more and more on the basis of articles they publish. From its earliest days, the Society has published important microbiology research – in its 75th year, our flagship journal Microbiology has published three papers by historian Peter Collins, detailing its fascinating story. Publishing has always been the main source of income for the Microbiology Society. The financial surplus that our journals generate funds our conferences, prizes, professional development activities and meetings. Rampant inflation makes life tougher for the Society just as it does for family budgets; the reason we have a financial buffer is the historic success of our journals. If the next five years are to be successful, if Council’s aim of a more inclusive Society with ever greater impact is to be realised, the journal titles will be crucial to that success. If you value the Microbiology Society, if you enjoyed Annual Conference or know someone who received a Harry Smith Summer Studentship, if you’d like to be on a Committee or if you think we can help with your professional development, the single easiest thing you could do to help is to submit your next research paper to one of our six journals, which between them provide a home for all microbiology.

Peter Cotgreave Chief Executive

p.cotgreave@microbiologysociety.org

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Protists on the spot: opening the field of view on protistology

Fiona Henriquez, Sonja Rueckert and Anastasios Tsaousis

Discovery of protists When it comes to the natural world, most knowledge, including that of the general public, is focused on animals and plants. Until a few centuries ago, one of the major reasons for this was the lack of technology to make micro-organisms visible. This changed when Antoni van Leeuwenhoek (1632– 1723), a trained linen draper and haberdasher, developed a single-lensed microscope out of his own interest to study what lay beyond his eyes. Leeuwenhoek spent a lot of time making lenses to find the perfect one. The range of magnification of these lenses was between 50 and 300 times. Driven by his curiosity, he used these simple microscopes to describe the little critters he discovered in environments that ranged from rainwater to the human intestine, as animalcules. Even though he was not a trained scientist, his thorough observations enabled him to make some fundamental discoveries, which he sent in the form of letters to the Royal Society. In the beginning, his discoveries were often disputed due to his background, but this changed over his lifetime, and his work (~375 contributions) was mostly published in Philosophical Transactions . He has been coined as the father of microbiology as his microscopes enabled him to describe bacteria and protists for the first time ever. He was motivated to answer essential questions, some of which we are still trying to answer today: why is there such a diversity (morphology/ behaviour) of these organisms and how did it evolve? How can they be distinguished and classified? Why is protistology important? Protists or protozoa are a large group of single-celled eukaryotes that have been identified across the eukaryotic tree of life. They are not a monophyletic group, and some species are close relatives of plants, animals and fungi.

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They contribute significantly to microbial ecology, soil fertility and water quality. They also have an enormous impact on animal and human health, with many species known as emerging pathogens. Protists interact with other microbes (viruses, archaea, bacteria and fungi) through predatory, mutualistic or symbiotic relationships. This makes the study of protists (protistology) an important node in the different fields of biology, including ecology, infectious diseases and evolution. Ecology. Protists have been isolated from diverse habitats, including extreme environments, such as polar regions, deserts or deep-sea ocean vents. Advances in protistology reveal new species and ecological interactions with other organisms. Their key roles in environmental niches highlight their importance in influencing environmental health. Infectious disease. Many human and animal obligate and opportunistic parasites are protists. They use different routes to transmit infections, e.g. through vectors ( Plasmodium, Leishmania, Trypanosoma) or the oral-faecal route ( Cryptosporidium , Toxoplasma oocysts, Eimeria, Entamoeba , Giardia ). A common challenge with all protist pathogens is the tremendous difficulty in treating and preventing the disease they might cause. In addition to causing infection, some protists are themselves vectors of infectious agents. For example, the opportunistic pathogen Acanthamoeba harbours pathogenic bacteria itself, such as Legionella . By contrast, some protists are described as key determinants in animal and plant health, due to their ability to phagocytose and therefore remove pathogenic bacteria.

Left: Antoni van Leeuwenhoek. Right: ‘Animalcules’ observed by Leeuwenhoek, ca 1795. Rijksmuseum (left); Ann Ronan Picture Library (right)/Science Photo Library

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Coloured scanning electron micrograph of a single Dictyostelium discoideum amoeba with bacteria. Eye of Science/Science Photo Library

researchers due to lack of time and expertise. Whilst modern omics technologies have allowed us to study communities, from molecules via species to the system level, they do not provide deep insights into the basic biology and ecology of protists. The strength of observations, that can be made with even the simplest microscopes like Leeuwenhoek developed and used, are not to be underestimated when it comes to understanding the biology and ecology of protists and should be a valid aspect in combination with new advanced technologies. With this Microbiology Today issue we would like to increase cross-sector awareness of the field of protistology, emphasising the role of protists in ecology, health, disease and evolution and their importance in the environmental and health sectors, including the benefits and challenges associated with their presence in certain niches.

Evolutionary biology. Protists are excellent models for understanding evolution. Their genomes often include evidence of lateral gene transfer, in particular from bacteria, archaea or other protists. This is no surprise in view of their intimate relationships with other micro-organisms. Genetic data strongly suggest protist–microbe symbioses, from the first studies identifying mitochondria, plastids and other organelles as products of early endosymbiosis of bacteria. Moreover, several protists, such as choanoflagellates, are used as models to understand the evolution of multicellularity. Modern technologies Over the last few decades, there has been an explosion of new technologies that have been used to understand the biology of all lifeforms. These ‘omic’ technologies have also revolutionised protistology research. Scientists have identified novel species at a rapid rate using a combination of single cell genomics, metabolomics and proteomics, and this has also increased knowledge of symbiotic relationships between protists and other microbes. Despite this tremendous progress in the field, the major challenge is to understand how protists survive, develop relationships with other microbes and adapt to new environments in a temporal manner. Traditional protistology includes cell culturing, single-cell isolations, staining and microscopy (from light to advanced electron microscopy), techniques that are slowly being ignored by

About the authors

Fiona Henriquez Professor of Parasitology, Infection and

Microbiology Research Group Leader, School of Health and Life Sciences, University of the West of Scotland, Lanarkshire Campus, G72 0LH, UK

Fiona.Henriquez@uws.ac.uk @FionaHenriquez

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More information about the authors, news and events regarding the society can be found on the Protistology-UK website ( protistology. org.uk ). What inspired you to get involved in protistology research? Fiona: During my honours project I started working on Toxoplasma gondii and I was fascinated by these tiny eukaryotic cells that could invade mammalian cells. During my PhD and postdoc I met researchers who were amongst the first to characterise protist life cycles and their role in the environment – this consolidated my enthusiasm for such fascinating micro-organisms. Sonja: I used to work on metazoan fish parasites, but then my postdoc supervisor, Professor Brian Leander at the University of British Columbia, Canada, introduced me to protists. Roughly since 2007, I was hooked, with a focus on a specific protist group, the gregarine apicomplexans. There are a lot of species described, some of which I actually described, but there is still so much to learn about these fascinating organisms. Anastasios: During my PhD studies I was introduced to the evolutionary cell biology field, where I was studying the adaptations of various single-celled parasites. A few years later, after attending my first protists’ meeting, I was really fascinated about the diversity, biology and adaptations of these organisms, which subsequently triggered my interest to work with them. Why is it important to be part of a membership society like Protistology-UK and the Microbiology Society? Fiona: Both societies are very welcoming and provide a great source for networking, news and skills development. Sonja: Membership societies provide you with the opportunities to interact with your research community. While it is clear that there is a lot knowledge exchange going on, e.g. at conferences, it is often the small conversations that you have or new people you meet that spark new research projects. There is also a lot of support offered, especially for young researchers to help them with their career paths, networking, skills development, and monetary help to attend scientific meetings, which are all extremely valuable Anastasios: Both societies provide great opportunities for networking and diversification of knowledge.

Sonja Rueckert Associate Professor in Marine Biology/ Parasitology, School of Applied Sciences & Centre for Conservation and Restoration Science, Edinburgh Napier University, Sighthill Campus, Edinburgh EH11 4BN, UK

s.rueckert@napier.ac.uk @SonjaRueckert

Anastasios Tsaousis Reader and Principal Investigator in Molecular and Evolutionary Parasitology, School of Biosciences, University of Kent, Giles Lane, Stacey Building, Canterbury, Kent CT2 7NJ, UK

A.Tsaousis@kent.ac.uk @ADTsaousis

All authors are currently elected committee members of Protistology-UK, a society that aims to promote the study, teaching and dissemination of all aspects of protistology, from ecological to medical and from subcellular to population studies. We have formed a long-term partnership with the Microbiology Society, which so far has proven successful in bringing together and sharing knowledge between communities for the benefit of our memberships.

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News

Microbiology Society is now a member of EDIS

We are pleased to announce that earlier this year the Microbiology Society joined the Equality, Diversity and Inclusion in Science and Health (EDIS) group as a member organisation. In line with one of our core values, welcoming anyone interested in microbes, their effects and their uses, we are delighted to be a part of this coalition of organisations working together to improve the science and health landscape. …we believe fostering and promoting greater diversity and inclusion amongst our membership will ensure we reach the full potential of microbiology research and the impact it has on our current societal issues. “ Professor Gurdyal Besra FMedSci FRS, President of the Microbiology Society By joining the EDIS group the Society has committed to contributing towards their objectives whilst contributing resources. Learn more about the EDIS group and their aims at EDISgroup.org .

Join us in celebrating the Society’s diversity for LGBTQ+ STEM Day LGBTQ+ STEM Day is an annual awareness day that celebrates diversity in sexuality and gender identity whilst also highlighting obstacles and challenges faced by LGBTQ+ scientists. To mark this year’s event, we are hosting an online discussion that will include the participation of openly LGBTQ+ scientists representing different career stages, both in academia and the biotech industry. We will talk about the challenges that LGBTQ+ researchers face in their careers and how they overcome these obstacles through community-building and learning from leaders in the field. We have a fantastic line-up of panellists and speakers: Professor Bryan Bryson (Massachusetts Institute of Technology, USA), Dr Anna Fagre (Bat Health Foundation, USA), Dr Kevin Maringer (The Pirbright Institute, UK), Dr Jason Mellad (Start Codon, UK), Charlotte Roughton (Newcastle University, UK) and Professor Michael Sauer (Institute of Microbiology and Microbial Biotechnology, Austria). The event is open to everyone and will take place virtually on 18 November 2022 from 15:00 to 16:30 GMT . Register on our website at microbiologysociety.org/QueerInMicro .

Protistology-UK Autumn meeting 2022 Protistology-UK will be hosting their Autumn meeting on 1–2 December 2022 at the Natural History Museum in London, UK. The hybrid meeting will focus on the theme of recognising the value of core methods, and how these methods should be retained and married with new methods. Find full details about the Autumn meeting and register to attend on the Protistology-UK website at protistology.org.uk/autumn-meeting-2022 .

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News

Microbiology 75 This year marks 75 years of our founding journal,

Supporting Open Access: the growth of Publish and Read The Society continues to expand its successful Publish and Read model, now facilitating Open Access (OA) at 270 institutions across five continents. The Society’s business model, created in collaboration with other membership organisations in the Society Publishers’ Coalition, enables libraries to repurpose subscription spend and simplify administration for OA publishing. Affiliated researchers are entitled to uncapped, fee-free OA publishing, including in our fully OA titles, and access to all content on the platform. The model continues to go from strength to strength, onboarding individual institutions as well as national consortia in the UK (JISC), Australia (CAUL) and Canada (COPPUL, BCI, CAUL-CBUA, OCUL). The Society is actively working to grow the reach of this transformative agreement as a key tool in its journey to a sustainable OA future. What’s more, by publishing with a Society journal, you will also support funding for our grants, events and activities for the community. Find out more at microbiologyresearch.org/ publish-and-read . Microbiology Society launches open research platform Our sound science journal, Access Microbiology , has re- launched as an innovative open research platform, embracing smart manuscript review tools, transparent peer review and Open Data. The Open Access platform offers a new service for members of our community to disseminate their work rapidly, transparently and rigorously, and is a home for all research outlets, not just traditional research. Access Microbiology welcomes work from all branches of microbiology and virology, including replication studies, negative or null results, interdisciplinary work and more. It is a symbol of the wider transformation that is to come at the Society towards a world of Open Science. The platform is now open for submissions – free to publish until June 2023 ( acmi.microbiologyresearch.org ).

Microbiology ( mic.microbiologyresearch.org ), and 75 years of publishing for the community. Throughout the year, there have been a series of activities celebrating this milestone, and we are pleased to highlight the second of three historical articles that are being published this year. ‘How Microbiology was run’ ( doi.org/10.1099/mic.0.001234 ) explores what was involved in running the journal, the challenges it faced at different times, and how a general microbiology journal fit in an evolving discipline. In line with the biennial bacterial cell–cell communication meeting which took place in June last year, Microbiology launched the Environmental Sensing and Cell–Cell Communication collection. Guest edited by Martin Welch (University of Cambridge) and Anugraha Mathew (University of Zurich), submissions are welcomed on microbial sensing and signalling pathways, quorum sensing, chemoreception, secondary metabolism, and the complex interplay between different sensory pathways. The final collection of the year will focus on the journal’s newer section category, Microbial Evolution, and aligns with the Understanding and Predicting Microbial Evolutionary Dynamics meeting. This collection and meeting are organised by Microbiology Senior Editor and Editors: Michael Brockhurst (University of Manchester, UK); Jenna Gallie (Max Planck Institute for Evolutionary Biology, Germany); James Hall (University of Liverpool, UK); Stineke Van Houte (University of Exeter, UK). More information on how to submit will be released soon, so keep an eye out! We would like to thank everyone who has supported Microbiology so far. We look forward to our Open Access future, which you can learn more about in Gavin Thomas’ article on page 75, and hope that you will join us on our journey and influence the future of Microbiology . From January 2023, all articles published in Microbiology will be Open Access. The Microbiology Society is a not-for- profit publisher, publishing for the community, and all journals income is invested back into the Society.

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News

Annual Conference 2023 The Microbiology Society Annual Conference 2023 will take place Monday 17 April–Thursday 20 April 2023 at Birmingham International Convention Centre. We plan to curate a diverse scientific programme featuring

scientific symposia, workshops, professional development sessions, Prize Lectures and Hot Topics, and much more. Registration and abstract submissions will open in October 2022, and updates can be found on the event webpage ( microbiologysociety.org/microbio23 ).

Upcoming grant deadlines

Date Grant 1 December 2022 Travel Grant for eligible members wishing to present at conferences or attend training events taking place between 1 January and 31 March 2023. Events can take place in-person or virtually. 20 November 2022 Society Supported Conference Grant to support members who wish to organise a conference (in-person or virtual) in any field of microbiology, either independently or in partnership with another Society. 20 February 2023 Harry Smith Vacation Studentships to support undergraduate research projects during summer 2023. 1 March 2023

Federation of Infectious Societies (FIS) Conference 2023 Following the success of FIS/HIS 2022 in September, the Society is pleased to announce we’ll be hosting the Federation of Infectious Societies (FIS) Conference 2023 on Tuesday 14–Wednesday 15 November in Edinburgh and one day for an online meeting (date to be confirmed). Find out more and register your interest on the event webpage at microbiologysociety.org/FIS23 .

Connect with the Microbiology Society on social media:

Travel grant for eligible members wishing to present at conferences or attend training events taking place from 1 April to 30 June 2023. Events can take place in-person or virtually.

@MicrobioSoc

@microbiosoc

For more information please visit the website ( microbiologysociety.org/grants ).

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Microbiology goes Open Access

The opening of 2023 marks a significant event in the history of the Microbiology Society, with the transitioning of its flagship and oldest scientific journal, Microbiology , to full Open Access (OA). While our sister journal Microbial Genomics has been OA since it started, this is the first of the Society’s long-established journals that is ‘flipping’ to OA.

arm of the Society: your membership fees only constitute a tiny proportion of the Society’s income. We in the journal leadership team have known this for many years and have been working hard to increase the visibility and reputation of Microbiology . Now we need you as members to help us, and there are two clear ways to do this. The first is that if you are working in an institution or organisation that is not signed up to P&R to lobby them to consider signing up. Pricing is tiered so that the conversion to P&R is as cost neutral as possible; for instance, at Tier 1, the lowest tier, the P&R deal is effectively paid back from the first OA article authors publish in Society journals that year. That is in any of our journals, right across the portfolio of microbiology, including our new journal Microbiology Access , which has open peer review and a focus on publishing all robust research data. The second, and single most important thing you can do as a member, is then to publish in our journals and encourage others to do the same. We will always need to publish, but let’s think a little more about where we publish and where the profits from those activities end up. Publish OA with us. Increase your impact. Expand your reach. Support your community. “ I’m delighted that my institution has signed up to P&R. It’s a requirement of my funder, but also a point of principle, that we publish our work open access. I know I can submit our manuscript to any of the Society’s journals without needing to have discussions with my line manager or librarian either before or, more awkwardly, after submission about how we might cover an article processing charge. Frank Sargent (Newcastle University, UK)

Claudio Ventrella/iStock

T here is nothing worse than putting your heart into a piece of written work, for it to be published, but then for hardly anyone to be able to read it due to a paywall and for its impact to not be truly realised. With the switch to OA and our Publish & Read (P&R) deals available from the Microbiology Society it is now easier than ever to publish in our journals so that your research and ideas can be heard. The advantages of your paper being published in an OA journal are clear. Its visibility is assured, meaning more people can read and download your paper, from a much wider audience, leading to more opportunity for citation as shown in the figure below. This wider inclusivity for readers outside traditional ‘subscription’ institutions is a massive benefit. The Society also removes the cost barrier for authors from countries covered by Research4Life to publish OA for free to promote their fields across the globe. For authors in neither P&R nor Research4Life institutions, you can pay the article processing charge (APC). While this is clearly the right thing to do, it is not without its risks for the Society. You may not be aware how dependent the Society is on income from journal subscriptions, which are now being replaced by our pioneering P&R model. It is critical that P&R is successful for the Society to continue to function as a charity supporting the science of microbiology in the UK and beyond. Annual Conference, grants, policy activities and much more are all supported primarily through the publishing

Visibility of OA articles

Usage and citations are key indicators of the impact of research articles: on average these metrics increased when published OA by the following factors.

Gavin Thomas Editor-in-Chief, Microbiology

Based on averages in all journals with citation data from Web of Science

75 Microbiology Today October 2022 | microbiologysociety.org

The trojan horse relationship between amoebae and bacteria

Ronnie Mooney, Elisa Giammarini, Jackie Parry and Fiona L. Henriquez

P redator–prey interactions are amongst the most significant driving forces of evolution throughout all kingdoms of life. Evermore complex strategies for predation or evasion continue to be uncovered, and perhaps the interactions with the biggest impact on life occur at the microbial level. The free-living amoebae (FLA) present an interesting group of protists that obtain much of their nutrients through the predation of other microbial species, in particular bacteria. The FLA are essential in the regulation of bacterial communities within soil and aquatic ecosystems, engulfing and feeding on captured bacteria in a process known as phagocytosis (Figure 1). Generally, the predation of bacteria by protists is considered beneficial, and as much as 60% of bacterial species are regulated by amoebic phagocytosis, promoting ecosystem health and diversity. The efficiency whereby the FLA and other predatory protists can reduce bacterial populations has been exploited in water treatment processes to improve water quality and reduce the presence of bacterial pathogens. What we often fail to consider, however, is the impact of these interactions on human health. As protists have evolved strategies to predate bacteria, bacteria have evolved strategies to evade protists. While bacterial predation is largely beneficial, generations of predation by FLA on bacteria have given rise to sophisticated strategies that allow bacteria to evade the phagocytic mechanisms employed by the FLA. The evasion strategies are complex and many; while some allow the avoidance of detection by the amoebae, others permit intracellular survival. Herein, we focus on those bacteria capable of surviving intracellularly within FLA (amoeba- resistant bacteria) and discuss how this ongoing evolutionary arms race may have far-reaching implications on human health, driving antimicrobial resistance, complicating detection of pathogens and influencing disease outcomes.

Our reliance on effective antimicrobials might prove to have severe long-term consequences unless we can formulate effective mitigation strategies to slow the spread of AMR in the environment. To do this, we need to understand the factors that drive the evolution of AMR. Industrial pollution, pharmaceutical manufacturing, aquaculture and agriculture are commonly cited factors influencing the presence of AMR within the environment, and rightly so, yet the wider interactions between different micro-organism groups are less considered. Horizontal gene transfer (HGT) is the transfer of genetic material between two micro-organisms. In bacteria, this transfer of genes promotes genetic diversity and is a major contributor to the spread of AMR genes throughout bacterial populations. Briefly, genes that confer AMR can be passed between bacteria, occurring more frequently when the organisms are in close contact. Organisms that possess these genes gain a selection advantage when exposed to specific antimicrobials within the environment, which may prompt further spread of the gene. Interestingly, the conditions that promote gene transfer can be amplified during intracellular survival within amoebae. The intracellular environment of the amoebae has been described as a ‘genetic melting pot’, an environment that serves to fast track the transfer of genetic material between engulfed organisms. The ingestion of multiple phagocyte-resistant bacteria results in a highly dense population of cells within the amoebae, increasing the likelihood that gene transfer events might take place. Additionally, intracellular survival within the amoebae might also serve to reduce exposure to environmental antimicrobials to sub-inhibitory levels, ultimately selecting for increasingly resistant bacteria. Recently, genomic analysis of intracellular bacteria within amoebae revealed that HGT events were ongoing within the amoebae and identified transferred genes important in antibiotic resistance, stress tolerance, amoeba– bacteria interactions and virulence. Interestingly, the gene transfer events are not uniquely between bacteria, with studies demonstrating the acquisition by amoebae of genes from bacterial symbionts that might aid in reducing oxidative stress.

The genetic melting pot – amoebae, bacteria and antimicrobial resistance

Antimicrobial resistance (AMR) is undoubtedly one of the most significant emerging threats facing human health.

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Bacteria within phagocytic vacuole

Acanthamoeba sp.

Pseudomonas sp.

Bacteria bound to pseudopodia

Figure 1. Predation of Pseudomonas aeruginosa by Acanthamoeba castellanii trophozoites. Bacteria are taken into the intracellular region of the amoeba via phagocytosis. Ordinarily, these bacteria are degraded and used as a food source; however, many species have evolved survival strategies that permit intracellular survival. Ronnie Mooney

in cooling tower disinfection are significantly less effective in killing bacteria when cells are co-cultured with amoebae. Heat treatment is also less effective against intra-amoebic bacteria; L. pneumophila can survive in temperatures as high as 90°C when internalised, posing a significant risk to facilities using heat treatment as a disinfection strategy. Commonly used contact lens biocides are woefully ineffective against certain amoebic species and as such can often fail to prevent corneal infections resulting from contact lens wear. The increased tolerance of bacteria within amoebae is something that requires consideration when implementing effective disinfection strategies and, while unexplored at present, it could be speculated that antimicrobial exposure at sub-inhibitory concentrations within amoebae could select for increasingly resistant bacteria, which in turn might be a contributing factor to rising levels of AMR. The amoebae ‘switch’ for VBNC bacteria Amoebae can also trigger physiological changes within bacteria that can increase resistance and limit detection. In times of environmental stress, bacteria can transition to a quiescent life stage better suited to the extracellular pressures they are exposed to. These bacteria are termed viable but non-culturable (VBNC) and have demonstrated an increased tolerance to many disinfectants as well as being able to evade culture-based detection. For reasons yet unknown, the conversion between the vegetative and VBNC stage can be triggered in both directions upon ingestion by FLA. In many instances, this intra-amoebic switch causes bacteria

Understanding these interactions will improve the efficacy of mitigation strategies and will be an essential aspect of combatting AMR globally. The microbial Trojan Horse Resistance to antimicrobials is not only facilitated by the increased likelihood of gene transfer events; the ability to resist phagocytosis and remain viable within the amoebae also directly limits exposure of the bacteria to the external environment and, as a result, exposure to antimicrobial therapies. Clinically, the implications of increased tolerability to antimicrobials within FLA is significant, particularly within high-risk areas such as artificial water systems or during food processing treatments. Amoeba can function as a microbial Trojan Horse, shielding pathogenic bacteria from the external environment and delivering them to a vulnerable human host. Indeed, Legionella pneumophila , Pseudomonas spp., Helicobacter spp., Mycobacterium spp., Aeromonas spp., Salmonella spp. and Escherichia coli have all been shown to survive within FLA after exposure to antimicrobial treatments. Many amoebae have an increased tolerance to commonly used disinfection strategies such as chlorine or heat treatment and as such can shield intracellular bacteria from the effects. Sodium hypochlorite, for example, is a commonly used disinfectant within hospitals and is often used in the treatment of potable water; research has shown, however, that killing intra-amoebic bacteria requires concentrations four times higher than is required for extracellular bacteria. Similarly, broad-spectrum biocides such as quaternary ammonium compounds used

77 Microbiology Today October 2022 | microbiologysociety.org

iStock/wir0man

been proposed that the same strategies which evolved over generations to evade phagocytic predation in amoebae have equipped bacteria for macrophage survival in the human body. For example, Legionella spp. can infect and kill both amoebae and macrophages, causing severe disease in human hosts. Moreover, Mycobacterium abscessus upregulates the secretion of the proteins that allow this bacterium to survive in a hostile environment and adapt to live intracellularly in FLA and consequently macrophages. Understanding how bacteria can survive within FLA can help dissect the pathogenesis of these bacterial infections. Conclusion The interactions between FLA and phagocyte-resistant bacteria present just one specific area in an almost endless supply of microbial interactions. Indeed, the interactions between amoebae and fungal or viral pathogens has not

to convert much quicker than is observed in the extracellular environment. For example, Aeromonas hydrophila has been shown to enter the VBNC form twenty days quicker within amoebae than it does alone; whilst in P. aeruginosa, the shift from the VBNC stage to the active state can occur in as little as two hours upon amoebic ingestion. Amoeba-driven VBNC conversion of bacteria is a fascinating by-product of their co- evolution and one that might prove to have significant clinical implications. Bacterial gymnasia: how amoebae alter the pathogenicity of bacteria Not only does the intimate relationship with amoebae protect bacteria from detection, disinfection and treatment, but it can also alter bacterial pathogenicity, allowing bacteria to become resistant to immune responses in their hosts. Amoebae and macrophages have similarities in phagocytosis. It has

78 Microbiology Today October 2022 | microbiologysociety.org

been discussed here, yet it is another aspect of an already complex web. The spread of antimicrobial resistance, disinfection efficacy, accurate detection and diagnosis and disease outcome are all influenced by cross-kingdom interactions; thus, it is imperative that as our understanding of these microbial relationships grows, so too does our approach to combatting the effects.

Jackie has been studying phagocytic processes in free-living protists (flagellates, ciliates and amoebae) since 1990. She specialises in receptor-mediated uptake of prey and its subsequent digestibility (or lack of it) and how this might influence the evolution of pathogenicity within bacteria in the environment.

Fiona L. Henriquez Professor of Parasitology, School of Health and Life Sciences, University of the West of Scotland, Lanarkshire Campus G72 0LH, UK

About the authors

Ronnie Mooney Postdoctoral Research Fellow, School of Health and Life Sciences, University of the West of Scotland, Lanarkshire Campus G72 0LH, UK

fiona.henriquez@uws.ac.uk @FionaHenriquez

Fiona has been researching free-living amoebae for approximately 20 years, with over 80 research outputs in the field focused on the development of new treatments and prevention measures for human and animal health, understanding how amoebae can be vectors for bacteria, and their distribution and impact in the environment. What inspired you to work in protistology? Ronnie: My inspiration for choosing a career in protistology began during my undergraduate degree. Despite originally studying zoology, I found myself more interested in the parasitic protists that infected animals than in the animals themselves. After hearing stories of brain-eating amoebae, mind controlling apicomplexans and immune evading kinetoplastids it was impossible to choose any other career path. Jackie: They were more interesting to look at down the microscope and they have obvious personalities! Fiona: Their capability to cause infection and the challenge to find effective treatments has inspired me to continue to work in this field. Elise: I discovered the passion for protistology as I found out that it was a field still quite unexplored and, having a curious nature, it brought up the challenge of the discovery. What is the most challenging part of your job? Ronnie: Finding the motivation to leave the lab and open my emails! Jackie: Balancing research with teaching and engagement commitments. Fiona: There are many aspects of protistology that are still unknown. We cannot culture them easily and this is challenging. Elise: To remember that there’s a world outside the lab and beyond the microscope. It’s not always easy to find a balance when you work on a such interesting field.

ronnie.mooney@uws.ac.uk @RonnieMooney

Ronnie is a postdoctoral research fellow. His research bridges biomedical and environmental sciences, investigating the interactions between amphizoic amoebae and their bacterial endosymbionts. He is interested in the role of these interactions in facilitating the spread of antimicrobial resistance and how this relationship can influence pathogenicity and detectability.

Elisa Giammarini PhD Candidate, School of Health and Life Sciences, University of the West of Scotland, Lanarkshire Campus G72 0LH, UK

elisa.giammarini@uws.ac.uk

Before becoming a PhD student, Elisa was awarded a Bachelor’s in Biotechnology and three Masters’ degrees in Biological Sciences, Management of Marine Resources and Advanced Biomedical Sciences. Elisa worked as a high school science teacher for four years then moved to Scotland from Italy four years ago, with the ambition to realise her dream of becoming a scientist.

Jackie Parry Professor of Protistology, School of Health and Life Sciences, University of the West of Scotland, Lanarkshire Campus G72 0LH, UK

j.parry@lancaster.ac.uk

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