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microbiologytoday
vol35| nov08
quarterly
magazine of
the society
for general
microbiology
bugs on bugs
microbial diseases of bees
fungal farmers of the insect world
wolbachia and gene transfer
shedding light on photorhabdus
an inside job – bdellovibrio
nature’s experiment – bacteriophages
contents
vol35(4) regular features
159 News 202 Schoolzone 212 Hot off the Press
166 Microshorts 206 Gradline 215 Going Public
199 Conferences 209 Addresses 218 Reviews
other items
196 National Subject Profiles
210 Obituary – Professor Chris Thurston
articles
168 Microbial diseases of bees 184 An inside job: Bdellovibrio
Travis Glare & Maureen O’Callaghan bacteriovorus
Bees play an essential role in the world’s ecosystems, but
microbial diseases are posing a big threat to these vital
Liz Sockett
These predatory bacteria hunt down and eat their fellow
insects.
organisms.
172 Ancient fungal farmers 188 Bacteriophages: nature’s most
of the insect world successful experiment
Garret Suen & Cameron Graham Hatfull
Currie Phages could well be the world’s biggest reservoir of
Leaf-cutter ants not only grow fungi to eat. They unidentified genetic material.
weed their ‘gardens’ and apply pesticides too.
192 1983: a vintage year for
176 Bacterial sequences in an pathogen discovery
invertebrate genome Robin Weiss
Julie Dunning Hotopp & Jason Rasgon Important findings about three major infectious
diseases were made 25 years ago.
Some arthropods and nematodes need their bacterial
inhabitants to survive.
220 Comment:
180 Photorhabdus: shedding light Scotoma in contemporary
on symbioses microbiology
Susan Joyce and David Clarke Howard Gest
Which amazing microbe can make nematodes glow in the Are some bacteria really ‘unculturable’? Probably not
dark and yet kill certain insects? according to this writer.
Cover image Macrophotograph of the head of a worker honey bee (Apis mellifera). Dr Jeremy Burgess / Science Photo Library The views expressed
Editor Dr Matt Hutchings––Editorial Board Dr Sue Assinder, Dr Paul Hoskisson, Professor Bert Rima––Managing Editor Janet Hurst––Assistant Editors Lucy Goodchild & Faye Stokes by contributors are not
Editorial Assistant Yvonne Taylor––Design & Production Ian Atherton––Contributions are always welcome and should be addressed to the Editor c/o SGM HQ, Marlborough House,
necessarily those of the
Basingstoke Road, Spencers Wood, Reading RG7 1AG–Tel. 0118 988 1809–Fax 0118 988 5656–email mtoday@sgm.ac.uk–web www.sgm.ac.uk
Society; nor can the
Advertising David Lancaster, Ten Alps Publishing, London Office, 10 Savoy Street, London WC2E 7HR–t 0207 878 2316–f 0207 379 7118–e david.lancaster@tenalpspublishing.co.uk
Regular feature images pp. 159 SGM; 203, 219 Comstock / Jupiter Images; 207, 213 Stockbyte; 209 Digital Vision / Getty claims of advertisers
© 2008 The Society for General Microbiology––ISSN 1464-0570––Printed by Latimer Trend & Company Ltd, Plymouth, UK be guaranteed.
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stu SGM is pleased to announce that Dr Stanley B. Prusiner, Committee. We have recently carried out surveys of BSF
Director of the Institute for Neurodegenerative Diseases learned societies with journal publishing interests, and of
at University of California, San Francisco, has accepted society members as authors and readers, to find out some of
the invitation to be the first recipient of the Society’s new the wider implications of the open access (OA) movement, and
Prize Medal. Amongst many awards, Dr Prusiner won the the state of awareness about the issues. This stems from the
Nobel Prize in Physiology or Medicine in 1997 for his work desire of some research funders, such as the Wellcome Trust
proposing an explanation for the cause of BSE (‘mad cow and Research Councils UK, that papers from work they have
disease’) and its human equivalent, CJD. He coined the funded should be made freely available online at or shortly
term prion, which comes from ‘proteinaceous infectious after the time of publication. The concern of publishers is that
particle that lacks nucleic acid’ to refer to a previously an increase in the proportion of articles with OA could lead to
undescribed form of infection due to protein misfolding. a loss of subscription income. Research funders have varied in
their willingness to provide money for author-side payments for
Dr Prusiner will deliver his Prize Lecture entitled Prion
OA, to replace this possible loss of subscription income. There
Biology and Disease on 1 April 2009 at the SGM Spring
appears also to be confusion about what mechanisms different
Conference at Harrogate (www.sgmharrogate2009.org.uk).
funders have set up to provide OA funds.
A special symposium on prion research will also take place
on the same day. The first survey indicated that publishing societies earn
surpluses on their journal sales, which they recycle to support
student grants, educational activities, advocacy and public
Back content awareness, and subsidized conferences. Publishing scientific
journals is of course a global business: on average, around 90%
of IJSEM goes of our institutional sales are ‘exports’. However, to take a UK
online perspective, the 14 publishing societies in the survey received
a total of £1,790k p.a. in subscription and other journal income
The whole back content of
from UK universities, but returned a total of £3,864k in direct
the journal, which started
support (grants, bursaries, conferences) and a further £2,299k
out as the International
in indirect support (educational and other charitable activities).
Bulletin of Bacteriological
If grossed up for all UK publishing learned societies, this clearly
Nomenclature and Taxonomy
would amount to a very substantial amount of support for our
in January 1951, becoming
education system and the students involved. It would be an
International Journal of
unfortunate example of the Law of Unintended Consequences
Systematic Bacteriology in
if this support was threatened by funders’ OA mandates which
1966 before being retitled
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NEW ENGLAND The back content of Journal of General Virology is already and UK funders’ policies, which is at www.bsf.ac.uk/journals/
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microbiology today nov 08 159
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Nobel Prize Council – new structure New elected members of Council
in Physiology A Special Resolution to amend the Society’s Articles of Association was passed at the The following will serve on Council for 4 years from 9 September 2008:
or Medicine AGM on 9 September 2008. This will enable implementation of the changes to the SGM’s
Professor Mark Harris
2008 governing Council that were described on p. 106 of the August issue of Microbiology
Today. With effect from the AGM to be held in 2009, Council will consist of six Officers
I graduated with a first class honours degree in Biological Sciences from Plymouth Polytechnic in
This year’s Nobel Prize 1983 and then undertook my PhD at the Institute of Virology in Glasgow, working with Ron Hay on
and the number of Ordinary Members will be reduced to six over the period from then
rewards the discoveries adenovirus DNA replication. After a postdoc at the NERC Institute of Virology in Oxford working on
to September 2011. Much of the business will be transacted by subcommittees. The new
of two viruses causing baculoviruses with Bob Possee, I moved back to Glasgow to the Department of Veterinary Pathology,
Articles are available on the website at www.sgm.ac.uk/about/articles.pdf
severe human diseases. switched from DNA to RNA viruses, and began working on the Nef protein of HIV-1 in the lab
of Jim Neil. After 5 years as a postdoc I obtained an MRC Senior AIDS Research Fellowship and
One half will go to Harald Council – July meeting highlights subsequently moved to Leeds in 1997, taking up a Lectureship post in what was then the Department
zur Hausen (German
The SGM Prize Medal in The Gambia where Sir Howard and his of Microbiology. Whilst retaining an interest in HIV, my lab has moved over almost entirely to the
Cancer Research Centre,
wife Kira carried out charitable work. study of hepatitis C virus. My research is focussed both on basic mechanisms of virus replication as
Heidelberg, Germany) Council devoted a significant amount of
well as virus–host protein interactions. Our funding comes from a variety of sources including research
for his discovery of time to careful consideration of nominations SGM finances councils, the Wellcome Trust and industry. I have always been a strong supporter of the Society – I am
human papilloma viruses for the new SGM Prize Medal to be Council approved the membership fees currently an Editor of Journal of General Virology and serve on the Virus Division committee. I welcome
causing cervical cancer. awarded in 2009. It was agreed that the and SGM journal subscription prices for the opportunity to make a further contribution to SGM activities as a member of Council.
The other half will be President should approach Dr Stanley 2009. These will increase by on average
shared between Françoise Prusiner and he has been pleased to accept Dr Gary Rowley
4 %.
Barré-Sinoussi (Institut (see p. 159). A more detailed appreciation Gary Rowley is a lecturer of bacterial pathogenesis within the School of Biological Sciences, University
Pasteur, Paris, France) and of Dr Prusiner’s work will be published in Laboratory-based microbiology
projects for medically qualified of East Anglia. He did his PhD with Professor Mark Roberts, University of Glasgow, and then moved
Luc Montagnier (World a future issue of Microbiology Today. to the Institute of Food Research, as a postdoc in Professor Jay Hinton’s Laboratory. He moved to UEA
graduates
Foundation for AIDS in 2007 to take up a Faculty position. His research interests focus on the environmental regulation of
Honorary Membership The Treasurer announced that there will be
Research and Prevention, bacterial virulence genes using the intracellular pathogen Salmonella Typhimurium as a model organism.
Council has bestowed Honorary a new grant scheme to support medically
Paris, France) for their Recent work has focused on investigating the role of the envelope stress response in pathogenesis and
Membership of the Society on Dr Volker qualified graduates taking up a career in
discovery of human the mechanisms that Salmonella uses to detoxify nitric oxide.
ter Meulen, Professor Emeritus for Virology medical microbiology. The grants will fund
immunodeficiency virus.
and Immunology, Universität Würzburg, and the consumables part of short-term research
See the article by Robin
President of the ‘Leopoldina’, Gesellschaft projects in a ‘home’ hospital or another host
Weiss on p. 192.
für Naturforscher und Ärzte, Sachsen- laboratory. Applications to the scheme are
invited for 2009; see www.sgm.ac.uk/
Congratulations to … Deaths
Anhalt, in recognition of his outstanding
2008 contributions to the molecular biology of grants SGM Education Officer Dr Sue Assinder on University’s Faculty of Science. Professor The Society notes
Address Book paramyxo- and coronaviruses and chronic Retiring members of Council
her appointment as Director of Education,
Liverpool School of Tropical Medicine.
Hunter has been Professor of Molecular
Microbiology for the past 13 years.
with regret the deaths of:
virus–host relationships, as well as for his The President thanked the retiring
A copy of the latest edition Professor Peter Gilbert
engagement in SGM activities, science member of Council, Professor Bert Professor David Baulcombe (University of Professor Richard James (Head of the
of the Society’s Address (University of Manchester),
management and international microbiology Rima, Queen’s University, Belfast, for his Cambridge) on winning the 2008 Albert School of Molecular Medical Sciences,
Book, giving contact details a distinguished expert on
promotion. highly appreciated input to the activities Lasker Basic Medical Research Award. Along University of Nottingham) on being
of members, should have biofilms and a member
Professor Sir Howard Dalton of Council. He also noted the significant with Victor Ambros and Gary Ruvkun, the awarded the SfAM Communications Award since 1974. Professor
been enclosed with your
contributions of Professors Iain Hagan award honours the scientists who revealed 2008 for raising the profile of his applied Gilbert was due to speak at
mailing of this magazine. Council was pleased to hear that SGM had
and Rick Randall, who had resigned from an unanticipated world of tiny RNAs that microbiology work to the public. the recent SGM meeting in
If you did not receive one, been remembered in the will of former
Council earlier in the year, before the end regulate gene activity in plants and animals. Dublin and the programme
please get in touch with President, the late Professor Sir Howard Douglas Kell, Professor of Bioanalytical
of their terms of office. Baulcombe made his discovery whilst was changed so that
the Membership Office Dalton FRS. The bequest of £2,000 will be Science, University of Manchester, who
probing how plants defend themselves Professor Michael Brown
(members@sgm.ac.uk). used to promote microbiological projects Ulrich Desselberger, General Secretary is to be the new Chief Executive of the
against viruses. could deliver a tribute. A
Biotechnology and Biological Sciences
Professor Nigel L. Brown, former Director Research Council. He is a leading figure in reception was also held to
SGM Staff of Science and Technology at the BBSRC the world of systems biology. honour Peter’s memory.
Congratulations to Stefan Sidorowicz and his wife Helen on the birth of a baby daughter Laura in July, and to Nicolas who has moved to the University of
Professor Hilary Lappin-Scott (University of Professor Christopher
Fanget and his wife Amina on the birth of a baby son Bilal in October. Edinburgh as Vice-Principal and Head of the
Exeter and SGM Scientific Meetings Officer) Thurston, a member since
College of Science and Engineering.
Farewell to Gemma Sims who worked here for a year to develop a microbiology teaching resource to meet the who will be taking up a new post at Bangor 1972, died in August after a
requirements of the new A levels. This should be ready for distribution to UK schools early in 2009. We wish Gemma well Professor Iain Hunter (University of University in January 2009 as Pro Vice long illness. A full obituary
in her new post as teacher of biology at Leighton Park School in Reading. Strathclyde) on his new post as Dean of the Chancellor for Research. appears on p. 210.
160 microbiology today nov 08 microbiology today nov 08 161
Grants
NEW! – Medical Trainee Support Grants Scientific Meetings Travel Grants
Funding for medical microbiology trainees (during This scheme is open to a range of early-career
foundation or specialist training) to carry out short lab- microbiologists resident within the EU, ranging from
based projects on a microbiological topic. The grant covers postgraduate students through to first postdocs and newly
a contribution towards consumables costs only. Closing appointed lecturers. Funding is tiered according to the
dates: 20 March and 25 September 2009. location of the meeting. The maximum grants are: UK (or
country of residence) – £200; within Europe – £350; Rest
Student Schemes of World – £500. These grants may also be used to support
GRADSchool Grants attendance on short courses.
Postgraduate Student Associate Members registered for a President’s Fund for Research Visits
PhD in a UK university can apply for funding to support the
Grants are available to support short research visits
full cost of course fees for a GRADschool. Students funded
(1–3 months) by early-career microbiologists resident
by Wellcome Trust, BBSRC, NERC, MRC or EPSRC are
within the EU, ranging from postgraduate students through
entitled to a free place on a GRADSchool course and should
to first postdocs and newly appointed lecturers. Funding is
not apply to this scheme. Applications, on the appropriate
limited to a maximum of £3,000. Retrospective applications
form, are considered throughout the year but must be
will not be accepted. Closing dates: 20 March and
made before booking a place on a course.
25 September 2009.
Student Meetings Grants
Public Understanding of Science Awards
Grants contribute towards travel, registration and
Are you planning any projects to promote the public
accommodation expenses for attendance at one SGM
understanding of microbiology? Have you got a National
meeting each year. Applicants must be Postgraduate
Science Week event in mind? SGM can help. Grants of
Student Associate Members resident and registered for a
up to £1,000 are available to fund appropriate activities.
PhD in an EU country or Undergraduate Members based at
Applications are considered on a first come, first served
a university in the UK or Ireland accepted to present work
basis throughout the calendar year.
the meeting. Closing date for Edinburgh: 27 March 2009.
Elective Grants SGM has a wide range of grant schemes to support
Funding for medical/dental/veterinary students to work microbiology. See www.sgm.ac.uk/grants for details
on microbiological projects in their elective periods. Closing and closing dates.
dates: 20 March and 25 September 2009. Enquiries should be made to the Grants Office, SGM,
Marlborough House, Basingstoke Road, Spencers Wood,
Vacation Studentships
Reading RG7 1AG (t 0118 988 1821; f 0118 988 5656;
The 2009 scheme is now open for applications. As
e grants@sgm.ac.uk).
described on p. 208, the scheme offers a great opportunity
for undergraduates to work on microbiological research
projects during the summer vacation before their final year.
Lister Institute Research
The awards, which are made by competition, aim to give Prizes 2009
students experience of research and to encourage them Applications are now invited applicant’s research proposal
to consider a career in this area. The studentships provide from young clinicians and and track record. Applications
support at a rate of £185 per week for a period of up to biomedical scientists for the may be in any area of
8 weeks. An additional sum of up to £400 for specific 2009 Lister Research Prizes. biomedical science or related
research costs may also awarded. Applications must be The Prizes offer £200,000 to areas. Further information
from SGM members on behalf of named students. be spent on the recipient’s and forms are available from
research in whatever way the Lister’s website (www.
The closing date for applications is 13 February 2009.
they choose, other than for lister-institute.org.uk) or
Student Society Sponsored Lectures personal salary, and therefore directly from the Institute’s
These cover the travel and other expenses of up to two provide unfettered research Administrator (secretary@
speakers on microbiological topics per Society each year funding. Prizes will be lister-institute.org.uk). Closing
at student society meetings. allocated on the basis of the date: 5 December 2008.
microbiology today nov 08 163
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Individual awards for 2008 have been made to two SGM members, Dr Annette Cashmore (University of Leicester) and
manual Dr Julian Park (University of Reading). The awards recognize and celebrate individuals who make a significant impact on the
• Download quality student learning experience.
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Report on first-year undergraduate practicals
• Request a quote This report is the outcome of a workshop held in April 2008 by the Centre to discuss first-year undergraduate work in the
• Place an order biosciences. Participants shared experiences of delivering practical classes where problem-solving, research investigation,
creativity and innovation are key features. Amongst several disciplines, the report describes five microbiology investigations
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THE GATEWAY TO MICROBIOLOGY TM
SGM membership subscriptions 2009
The following rates were agreed at the AGM of the Society on 9 September 2008.
Membership category Annual Additional subscriptions for publications (print only)
www.labm.com subscription Microbiology JGV IJSEM JMM
£ US$ £ US$ £ US$ £ US$ £ US$
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microshorts
Lucy Goodchild takes a look at some stories Historical research
that have hit the headlines recently. highlights
The entire back-catalogue of IJSEM is now
GM cotton Scientists discover online – here’s a snippet from the content.
reduces pest ‘virophage’ 2005: Scientists identify olive fly
symbiont after 96-year search
damage Scientists have discovered a virus that can be infected by another
virus, according to research published in Nature. The giant virus, In 1909, Petri described an example of
A 10-year study by scientists called mamavirus, infects amoebae. When researchers from the hereditary symbiosis in the olive fly after
at the Chinese Academy of Université de la Méditerranée in Marseille, France, studied the observing unidentified bacteria under a
Agricultural Sciences in Beijing virus using an electron microscope, they discovered an associated microscope. He suggested that the
has revealed that the benefits virus, which they called Sputnik. This smaller virus is incapable symbiont might be Bacterium (Pseudomonas)
of genetically modified cotton of infecting cells on its own. As it has only 21 genes, Sputnik savastanoi, which causes olive knot disease,
extend further than had hijacks mamavirus machinery in order to infect cells, so it has as it could be isolated from the larvae.
previously been anticipated. been dubbed a ‘virophage’. By hijacking it, Sputnik reduces Petri postulated that the bacterium might
Cotton modified with a gene the infectivity of mamavirus. Giant viruses are able to infect be unculturable, a speculation that has
from Bacillus thuringiensis climatically important plankton, which produce dimethylsulfide. remained the case for almost a century. In
to make its own insecticide Therefore, by reducing the infectivity of mamavirus, Sputnik virus 1965, Buchner analysed the bacterium,
was able to resist attack could potentially affect climate change. m Two variants of the Harlequin ladybird. Sheila Terry / Science Photo Library followed closely by Hagen in 1966, but
from its biggest pest, the www.nature.com/news/2008/080806/full/454677a.html neither disputed Petri’s designation.
cotton bollworm. The study,
published in Science, showed Ecologists find invasive ladybird’s In 2005 Capuzzo et al. from Università di
Padova and Università di Udine in Italy
that the GM crop resulted in
a ‘dramatic long-term decline’
Bar-coding midges to stop Achilles’ heel proposed the novel species ‘Candidatus
Erwinia dacicola’. By sequencing the entire
in damage. The pest-resistant
crop even reduced the
spread of bluetongue The Harlequin ladybird was introduced to the UK 4 years ago as a form of biological
control of aphids and it has since become an invasive species, posing a major threat to 16S rRNA gene, they were able to show
Scientists have developed a method of genetically ‘bar-coding’ native ladybirds. The Harlequin is larger and more aggressive than native ladybirds and is marked similarity with enterobacterial
cotton bollworm population
biting midges that could help prevent the spread of bluetongue also resistant to a deadly fungus, Beauveria bassiana, that threatens native species. Although lineages, with close matches to Erwinia
in neighbouring fields, a
m Cotton bollworm caterpillar. Nigel Cattlin / disease. Researchers from the University of Aberdeen collected 1 Harlequin ladybirds do not succumb to infection with the fungus, the number of eggs they persicina and Erwinia rhapontici.
surprising result
SPL million midges in 37 light traps lay after exposure to the pathogen is dramatically reduced. However, because the fungus is Adults of the olive fly Bactrocera oleae, the
for the researchers.
in Scotland between late 2007 so deadly to the already endangered native ladybirds, it is not a viable means of controlling most important pest of olive trees, carry the
c Biting midge (Culicoides sp.) feeding on www.timesonline.co.uk/tol/news/uk/
and early 2008. They used a the invaders. Speaking at the British Ecological Society’s conference at Imperial College bacteria in an organ called the oesophageal
human blood. Sinclair Stammers / SPL science/article4783078.ece
pioneering DNA test to identify London, scientists say they are now looking at semiochemicals, which the insects use for bulb. The bacteria replicate rapidly and
the midges Culicoides obsoletus, communication, to control Harlequin ladybirds. form masses that reach the midgut. The
Vaccines for bacteria C. chiopterus, C. dewulfi and C.
scoticus, and create a map of
www.alphagalileo.org/index.cfm?fuseaction=readrelease&releaseid=531792 mother transmits the bacteria to her eggs
during oviposition, then the bacteria
Bacteria used in industrial processes could be protected from their geographical distribution
virus infections using a kind of vaccine, according to research in Scotland. In southern Mosquitoes lured by odourless multiply inside the larvae. By rearing
the flies on artificial media, the scientists
chemical
published in Science. German researchers at Wageningen University Europe, Culicoides imicola carries
observed that the progressive loss of the
uncovered the mechanism some bacteria use to defend themselves various strains of bluetongue
symbiotic bacteria resulted in lower vitality
in the long term against potentially lethal viruses: this has potential virus and is responsible for its Catching mosquitoes is a key part of the low doses and extensive field research in and fertility of the flies. Furthermore, flies
to protect good bacteria and target pathogenic species. Bacteria spread across the continent. surveillance of vector-borne diseases like Brazil showed it is as effective as the lure lacking the symbionts were more prone to
insert pieces of viral DNA into their own genome. The ‘adopted’ However, the virus has been West Nile virus, encephalitis and lymphatic currently used. Gravid female traps target infection by other microbial species.
segment is used like a snapshot to help the bacterium remember found in different midge species filariasis. People who monitor the mosquito mosquitoes that have fed on blood and
the virus and kill it during a subsequent infection. The researchers in the UK and scientists are traps, and even those who live near them, are ready to lay eggs. Because mosquitoes Although the evidence suggests a symbiotic
identified six bacterial proteins involved in the defence system; one tracking them to gauge the have to suffer the highly offensive smell lay hundreds of eggs at a time, catching relationship between the bacteria and
cuts the ‘adopted’ segment out of the bacterial genome and helps speed at which the virus might of the attractants currently in use. Now, females ready to lay can reduce the number the olive fly, the bacteria still could not
the other five proteins to compare it to the DNA of the invading spread if it reaches Scotland. scientists at the University of California, of mosquitoes capable of spreading be cultured. However, the availability of
virus. This mechanism could be utilized to protect industrially The study revealed that midge Davis in the USA have developed a diseases dramatically. The research could modern DNA-based methodologies allowed
important bacteria from being attacked by bacteriophages. It numbers were dependent low-cost attractant that lures mosquitoes play a key role in surveillance and control the researchers to succeed where Petri had
could also be targeted to combat antibiotic-resistant bacteria; by on climatic and geographic without making humans hold their programmes for Culex mosquitoes. not: to clarify the systematic placement of
deactivating the system, bacteria would be left defenceless and conditions. noses; it is odourless to us, but enticing the microbes and to trace their connections
www.newspostonline.com/sci-tech/killing-
susceptible to bacteriophage attack. www.alphagalileo.org/index.cfm?fuseact to mosquitoes. The synthetic mixture mosquitoes-without-raising-a-stink-just-became-a- to related species.
www.alphagalileo.org/index.cfm?fuseaction=readrelease&releaseid=531517 ion=readrelease&releaseid=531840 contains trimethylamine and nonanal in reality-200808313789 IJSEM 55, 1641–1647 (doi: 10.1099/ijs.0.63653-0)
166 microbiology today nov 08 microbiology today nov 08 167
Microbial
diseases
T
he humble bee has a special collapse of bee colonies. The name
place in our lives. Essential describes the symptoms of diseased 1
for pollination of many plants, brood; infected cells become dis-
of bees
including food crops, the coloured, sunken and there is a char-
provider of honey and royal acteristic smell. Adult bees are not
jelly and many other products, affected. This disease has traditionally
bees are important to the economies been treated with the antibiotic oxy-
of countries and, as ecosystem tetracycline, but some bacterial strains
service providers, have few equals have developed resistance to this and
among insects. There is a quote, often the disease is now increasing in preva-
attributed to Einstein, suggesting that lence around the world. Although the
if all the bees disappeared then disease was first described over 200
humans would follow within 4 years. years ago, much is still unknown about
While this is perhaps an overstate- this infection. A German research team
ment, a recent estimate of the has only recently discovered how the
contribution of insect pollination, bacteria kill larvae, by building up to 2
mainly by bees, to agriculture was very high numbers in the gut before
€153 bn. bursting into the haemocoel, causing
There are many threats to bee death.
survival, including the risk of disease European foulbrood (EFB) is caused
caused by micro-organisms. The vast by the non-spore-forming bacterium
majority of our knowledge of bee Melissococcus (=Streptococcus) plutonius.
diseases focuses on the honey bee, Apis Unlike AFB, EFB usually affects
mellifera, although there are actually unsealed brood, and the recently dead
over 20,000 species, both stingless larvae present as watery and yellowish
and stinging, from those with solitary brown cadavers twisted inside the cell.
lifestyles to complex societies such as Despite the importance of EFB, the
honey bee hives. disease is poorly understood, but like
Viruses, fungi, protozoa and bacteria AFB, has increased in prevalence in
are all known to cause infections in recent years.
3
bees, sometimes leading to collapse of Of the fungi known to infect bees,
colonies, and causing serious threats species of the fungus Ascosphaera are
to the bee-keeping industry. Bees have the most common. Ascosphaera apis is
two distinct life forms, brood (egg, larva the causative agent of the well known
and pupal stages which develop within chalkbrood disease in honey bees, so
the hive) and adult. Most diseases are called because of the chalky appear-
specific to just one of these life stages. ance of infected brood. Chalkbrood is
While the list of diseases is quite long, usually considered a minor disease of
only a few are of serious concern to bees, as is stonebrood, caused by the
apiculturists. fungus Aspergillus.
Bees come under attack Viruses can also cause devastation
Major disease of bees in bee colonies. At least 18 types of
Various evocative names, based on the
from a wide range of microbes. visual symptoms of diseased bees, are
viruses have been found infecting
honey bees alone. Going by some
m 1. Sunken brood capping with holes suggests
used to describe the most problematic delightfully descriptive names (e.g. American foulbrood (AFB). Zachary Huang, Michigan
Travis R. Glare and Maureen diseases, for example foulbrood, sac- deformed wing virus, chronic paralysis State University, USA
brood and chalkbrood. virus, acute bee paralysis, sacbrood 2. A dead larva killed by AFB usually forms a ‘false
American foulbrood (AFB) is caused virus and black queen cell virus), tougue’ pointing upward. M.V. Smith, University of
O’Callaghan consider the role of bee by the spore-forming bacterium Paeni- these viruses range from non-lethal to
Guelph, Canada
3. Larvae showing typical European foulbrood (EFB)
bacillus larvae. The disease was first causing significant mortality in nests. symptoms. These larvae show yellow streaks. M.V. Smith,
diseases in the worldwide decline of described in 1769. AFB is probably One of the more interesting aspects University of Guelph, Canada
the most virulent disease of honey bee of viral disease is that many infections b A honey bee (Apis mellifera) feeding. Dr John
brood and is capable of causing the cause no obvious symptoms much of Brackenbury / Science Photo Library
these key ecosystem providers.
168 microbiology today nov 08 microbiology today nov 08 169
1 2 3 4
m 1. Chalkbrood, whereby the larvae become mouldy with white (adult) honey bees on several continents, especially North detected in the semen of honey bee others. Some strains of bees are capable understanding of the cause of CCD,
hyphae, then hardened to be similar to pieces of white chalk. This
America. The sometimes startlingly high mortality rates have drones, suggesting that mating may of recognizing diseased brood well no cure will be possible, but when
disease is mostly considered a stress disease, only occuring in weak,
or in otherwise stressed colonies. M.V. Smith, University of Guelph, not been attributed to a particular cause. Several recent spread some disease both horizontally before it is a threat to the hive, and the factors are known, many large and
Canada studies suggest that some colony collapse is caused by a and vertically. Pathogens can be remove diseased individuals. In some small mitigations can be used.
m 2. Close-up of the head of a larva killed by Sacbrood. M.V. Smith, combination of disease and the parasitic attentions of Varroa transmitted in bees and sometimes cases, the task of disposing of diseased The risk is that with increasing
University of Guelph, Canada mites. Various studies have found that prevalence of viral in bee products, prompting many insects falls to specialist ‘undertaker pressure from civilization, bees could
c 3. A honey bee (Apis mellifera) with two Varroa jacobsoni mites on and protozoan diseases is higher in Varroa-infected hives countries to closely regulate the bees’ that appear to be old workers. suffer increasingly from threats and
its thorax. Maryann Frazier / Science Photo Library
and Varroa is thought to be capable of acting as a vector importation of bees and honey. Bees are also assisted in resisting dis- stress, including increasing prevalence
c 4. Coloured SEM of a Varroa sp. honey bee mite. Steve Gschmeissner
for pathogenic microbes. In some cases, viral diseases that ease by propolis, present in the of disease. A better understanding of
/ Science Photo Library
do not usually cause high mortality are rampant in hives How do bees defend plant resins collected by honey bees bee dynamics and the development
with Varroa or have been associated with CCD. Israeli Acute themselves from disease? and used as a sealant in the hives. of mitigations is urgently required.
the time. Kashmir bee virus can persist in bee populations Paralysis Virus (IAPV) was recently found to be the most The high density populations and Propolis is known for its antimicrobial
causing no obvious symptoms, only to explode into lethal consistent indicator of CCD, as well as Kashmir bee virus conditions within the bee colony properties. Travis R. Glare & Maureen
infections, possibly triggered by bee stress factors such as and Nosema spp. However, no causal link has been made (enclosed, moist, dark, poorly venti- O’Callaghan
attack by the Varroa mite. Varroa mites are parasites on honey between IAPV and CCD. As with all living things, stress lated) are ideal for the outbreak What hope is there for AgResearch, Lincoln, Private Bag
bees and have spread around most of the world, causing increases the susceptibility of the host to a pathogen, and and spread of disease. Fortunately, the future? 4749, Christchurch, New Zealand
significant losses in hives as well acting as vectors for some if bees are under stress, disease can be more debilitating. because bees are constantly exposed With increasing prevalence of disease,
(t +64 3 321 8825; e travis.glare@
viruses. Virus infections can be hard to detect and diagnose, Whether CCD is only caused by the interaction between to pathogenic micro-organisms, they unexplained disappearance of bees on
agresearch.co.nz)
as symptoms, if any, resemble other mortality causes. a specific stress such as Varroa and some diseases, or have evolved strategies to resist infec- some continents and the emergence
widespread interaction between a number of stresses is tion. The cuticle of bees acts as a barrier of new diseases, bee populations are
Emerging diseases unclear. Combinations of stresses could include multiple to penetration, and immune system- under threat. Fortunately, increasing Further reading
Bailey, L. (1968). Honey bee pathology.
Microbes are constantly evolving, leading to the emergence diseases. Using molecular techniques, several studies have based defence can prevent infection sophistication of research methods is
Annu Rev Entomol 13, 191–212.
of new strains with novel pathogenic abilities. For example, shown multiple diseases infecting single bees. So diseases, of many minor pathogens. However, allowing unprecedented understand-
some honey bee diseases appear to have widened their host some of which may not normally cause death, could act the recent completion of the honey ing and insights into bee pathology Chen, Y.P. & Siede, R. (2007). Honey
range in recent years. Protozoa of the genus Nosema infect together to kill. Additionally, nutritional stress can exacerbate bee genome sequence has shown that by allowing detection of cryptic bee viruses. Adv Virus Res 70, 33–80.
many invertebrates, and individual species are typically the incidence of pathogens. they have only about a third of the infections, generation of epidemiolo- Cox-Foster, D.L. & others (2007). A
quite limited in their host range. Nosema apis has long been number of known immunologically gical data and detailed understanding metagenomic survey of microbes in
recognized as causing one of the most important diseases How do diseases spread? related genes when compared to flies of bee–pathogen interaction. With honey bee colony collapse disorder.
in adult honey bees, infecting the guts of adult bees. How- How diseases spread between individuals is still largely or mosquitoes, suggesting that bees increasing understanding comes a Science 318, 283–287.
ever, Nosema ceranae, thought to infect only the Asiatic or unknown. Both horizontal transmission (where viruses are rely less on individual immunity than better appreciation of the role of dis- Evans, J.D. & others (2006). Immune
Eastern honey bee, Apis cerana, has recently been shown transmitted among individuals of the same generation), and most insects. ease and methods for reducing impact. pathways and defence mechanisms in
to infect the European honey bee, A. mellifera. Evidence vertical transmission (where the disease is passed from Bees, in common with a number of For example, the presence of Kashmir honey bees Apis mellifera. Insect Mol Biol
is emerging of recent spread of N. ceranae in honey bee queens to their offspring) are known. Modern molecular- other social insects, have well devel- bee virus has been detected in the 15, 645–656.
populations around the world since around 1998. There based techniques have contributed significantly to our oped behavioural responses to combat UK, despite never being identified as Paxton, R.J. & others (2007). Nosema
is ongoing risk that other highly virulent diseases of honey understanding, allowing investigation of whether pathogens disease. These behavioural responses a cause of infection in UK bees based ceranae has infected Apis mellifera in
bees will emerge. are present inside eggs, and by establishing the relatedness are collectively known as hygienic on visual symptoms. This suggests a Europe since at least 1998 and may
of occurrences of disease in different hives. It is obvious behaviour and include recognition and potential non-lethal role for this virus. be more virulent than Nosema apis.
Bees under stress how some diseases spread; the presence of large numbers removal of diseased brood by worker Detection of virus associated with Apidologie 38, 558–565.
There is still so much we don’t know about how combinations of spores, whether fungal, bacterial or protozoan, inside a bees. Bee species, and even different CCD may also lead to a cure. Wilkins, S. & others (2007). The
of microbial diseases, parasites, pollution and urbanization hive will contaminate brood and/or workers that come in hives of the same species, differ in their Separating the various factors affecting incidence of honey bee pests and
are affecting bees. Colony Collapse Disorder (CCD) is the contact. However, some more unusual routes have also ability to perform hygienic behaviours, bee colonies will allow the causal diseases in England and Wales. Pest
name given to the recent widespread mortality of worker been demonstrated. DNA from viral pathogens has been with some colonies far superior to agents to be directly treated. Without Manage Sci 63, 1062–1068.
170 microbiology today nov 08 microbiology today nov 08 171
Ancient
fungal
farmers
of the Not only humans practise agriculture.
As Garret Suen and Cameron R. Currie
insect describe, ants have amazing systems of
growing fungal crops in their ‘gardens’ too.
world b A worker of the leaf-cutting ant Acromyrmex octospinosus tends to her fungus garden. These
ants grow bacteria on their body and use the antibiotics the bacteria produce to protect their
gardens against infection from invading pathogens. Heidi Horn
T
ake a stroll through a rain forest in South America not cut leaves, but instead collect fruit, the colony produces male and female
and you might find yourself walking in a river, not leaf litter and decomposing organic winged reproductives called aletes,
of water, but of leaves. Leaf-cutter ants swarm in the material, such as caterpillar dung, to which mate in a spectacular display
underbrush, carrying their precious cargo back to grow their fungus. of flying ants. The newly-mated queens
their nest with an apparent single-minded deter- Fungus-growers also have diverse then go on to found new colonies.
mination. This conspicuous behaviour has made colony sizes, with some species con- Young queens transport a small piece
these ants one of the most dominant herbivores in the Neo- taining only a few hundred workers, of the fungus garden in a special organ
tropics, and one of the most successful social insects in nature. while many leaf-cutting ant species known as an infrabuccal pocket when
A closer look at the ants reveals that they are ancient farmers, can contain upwards of 5 million. All they leave the nest for their mating
having developed the secret of agriculture over 50 million species, however, follow the same life flights, and thus ensure that they can
years ago. Using their freshly-cut leaves, they incorporate cycle. Organic material is brought into successfully start a fungus garden in
them into gardens where they grow a specialized fungus the colony by foragers and is then the new colony.
that they consume for food. This relationship between ant processed to form a garden matrix
and fungus has been described as a breakthrough in animal where the fungus grows. New material Garden microbiology
behaviour, and parallels the practice of sustainable agriculture is continuously incorporated into the Until about a decade and a half
in humans, arguably the most important development in gardens in order to propagate the ago, research on fungus-growing ants
human civilization that, in our opinion, resulted in the fungus, and old material is removed focused primarily on the ants and their
dominance of humans on planet Earth. by the ants and placed in special refuse foraging behaviour. It wasn’t until the
Leaf-cutting ants are the most highly-derived group of ants dumps away from the colony. In many early 1990s that this focus shifted to
that practice fungus growing. A total of four other fungus- groups of fungus-growing ants, the the fungus gardens and their associated
growing ant agricultural systems have been described, fungus produces specialized packets microbial communities. Since the
spanning over 200 different species of ants, each based on of nutrients called gongylidia that the ant gardens are maintained in soil
the type of fungus grown and the material incorporated into ants eat and feed to their developing chambers, they are routinely exposed
their gardens. The vast majority of fungus-growing ants do brood. At the start of the rainy season, to a number of potential pathogens
172 microbiology today nov 08 microbiology today nov 08 173Farming ants
The fungus feeds on a supply of freshly
cut leaves brought by the farming ants.
Acromyrmex
Lepiotaceae
Fungus crop
The fungus crop provides the
ants with nutrient-rich food.
b Fig. 1. The fungus-growing ant system.
The ants grow a fungus crop for food
in gardens, which often get attacked by
invading crop pests. The ants deal with
these attacks by growing bacteria on
the surface of their bodies that produce
antibiotics capable of stopping the pest.
Cara Gibson & Angie Fox
Bacteria Crop pest . Fig. 2. A fungus garden from a 1-year-old
Bacteria that grow on the surface of ants’ bodies Like human farmers, the ants can’t
produce an antibiotic that attacks the crop pest. keep their crops free of disease colony of Acromyrmex echinatior. Note that
They stop the pest from destroying the crop. organisms. An invading pest called many of the garden workers are covered
Escovopsis infects the fungus crop. with the antibiotic-producing bacteria.
David R. Nash
Escovopsis
c Fig. 3. Rivers of leaves. Foragers of the leaf-
cutter ant Atta cephalotes bring freshly-cut
leaves back to their nest. Alexander Wild
that could infect and overtake a garden. Mutualism happens
In fact, many of the ant colonies The interaction between the ants and their fungus crop, infects the gardens of the ants they are associated with.
do become overgrown by fungal and the ants and the bacteria is known as a mutualistic Interestingly, the tight association between ant, bacteria and
pathogens, often resulting in the death relationship. In general a mutualism is established when pathogen will sometimes result in the pathogen winning.
of the colony. Intensive sampling of both members of the interaction derive a benefit from the This interplay has been described as a chemical ‘arms race’
the fungal communities within the gar- association. In the ant–fungus mutualism, the ants obtain between the bacteria and fungus, with one side beating the
dens revealed that a specialized micro- nutrients from the fungus, and use this to feed the entire other as new compounds are evolved. At the moment, we are
fungal pathogen selectively attacks colony. This mutualism is so tight, that the loss of fungus beginning to understand the chemical warfare at the genetic
the gardens of the fungus-growing by the ants results in the death of the entire colony. In level, and it is likely that these types of interactions are more
ants. These fungi, which belong to the return, the fungus receives a continuous supply of growing prevalent in nature than previously thought.
genus Escovopsis, directly attack and material, protection from the environment, and the removal So how exactly does an ant go about forming partnerships
kill the crop fungus, and can overrun of disease-causing agents and competitors through the with a fungus and a bacterium? No one really knows. With
the garden in a similar fashion to the ants’ weeding behaviour and pesticide application. new advances in molecular and genetic technologies, such
way weeds and pests can ruin human So what do the bacteria get out of producing pesticides as whole-genome sequencing, we will hopefully begin to
gardens. for the ants? For starters, they get food. Many species of understand how these associations were established, and
A curious observation that researchers fungus-growing ants have evolved special crypts on their gain further insight into how these interactions resulted in
noted was that some workers had a bodies where the bacteria live and grow. It is thought that the remarkable fungus-growing ability of the ants.
white wax-like substance across the ants provide nutrients to the bacteria through glands
their bodies. It was thought that this connected to these crypts. Furthermore, the bacteria gain Garret Suen & Cameron R. Currie
substance was a wax produced by the a protected environment in which to grow, away from the Department of Bacteriology, University of Wisconsin-
ants themselves, with an unknown intense competition they would face if they lived in other Madison, Madison, Wisconsin 53706, USA
function. However, when viewed un- environments such as the soil. Since the ants are invested in (e gsuen@wisc.edu; currie@bact.wisc.edu)
der a microscope it was discovered that these bacteria as a producer of pesticides, they are carried
this covering was not a wax, but a by young queens that found new nests, and thus gain access
bacterium! Isolation of these bacteria to new resources that ensure their continued existence and Further reading
Currie, C.R. (2001). A community of ants, fungi, and bacteria:
revealed that they belong to the genus worker ant bodies is correlated to the onerous task! When Escovopsis is survival.
a multilateral approach to studying symbiosis. Annu Rev Microbiol
Pseudonocardia, which are part of the incidence of infection. At the onset detected by garden workers, there is
55, 357–380.
actinobacteria, a group of prokaryotes of invasion by Escovopsis, the actino- an immediate flurry of activity as ants A chemical arms race
that produces over 80% of the anti- bacteria will cover the workers’ bodies, begin to comb through the garden Research in our laboratory has revealed a number of interest- Currie, C.R., Scott, J.A., Summerbell, R.C. & Malloch, D.
biotics used by humans. Further work presumably to increase the production matrix. Upon finding the pathogenic ing properties between the bacteria and the pathogenic (1999). Fungus-growing ants use antibiotic producing bacteria
to control garden parasites. Nature 398, 701–704.
on this ant-associated actinobacteria of the pesticide. This discovery was fungus, they weed them out and fungus. The bacteria appear to be specially suited to
has shown that it produces antifungal the first demonstrated example of discard them into their refuse dumps inhibiting the pathogenic fungi that infect the ants’ fungus Currie, C.R., Poulsen, M., Mendenhall, J., Boomsma, J.J. &
compounds that inhibit the specialized an animal, other than humans, that away from the garden. By weeding garden. Even though these parasitic fungi belong to a single Billen, J. (2006). Coevolved crypts and exocrine glands support
microfungal pathogen that attacks the employ bacteria to produce antibiotics and applying pesticides, the ants genus, they are differentiated into various species and strains mutualistic bacteria in fungus-growing ants. Science 311, 81–83.
garden. As a result, it is now known in order to deal with pathogens. have developed a system to keep their that are each associated with particular groups of ants. We Poulsen, M. & Boomsma, J.J. (2005). Mutualistic fungi control
that these ants employ these bacteria as As a second line of defence, the gardens pest-free, an impressive feat have found that the actinobacteria associated with any crop diversity in fungus-growing ants. Science 307, 741–744.
a source of pesticides to control the in- ants have also adopted the practice of given that they grow their fungal crop given species of fungus-growing ant is effective at inhibiting Schultz, T.R. & Brady, S.G. (2008). Major evolutionary
vading pathogenic fungi. Interestingly, weeding. Anyone who has ever weeded in monoculture, an ability which has some strains of pathogenic fungi, but not all; they tend to be transitions in ant agriculture. Proc Natl Acad Sci U S A 14,
the spread of the actinobacteria on a garden can readily identify with this evaded human agriculturalists. most effective against the pathogenic fungus that specifically 5435–5440.
174 microbiology today nov 08 microbiology today nov 08 175The genomes of
many nematodes
and arthropods
Bacterial contain bacterial
sequences. How did
sequences in they get there? Julie
C. Dunning Hotopp
an invertebrate and Jason Rasgon
explain.
genome m Wolbachia infect the most abundant animal
phyla including nematodes and arthropods.
This includes some bees and butterflies like
those shown here. J.C. Dunning Hotopp
W
olbachia pipientis is the most prolific into reproductively capable females, and (4) cytoplasmic Unlike infections in arthropods, that Wolbachia provide the host with the obligate symbioses between these
intracellular endosymbiont on earth. incompatibility, the most common phenotype, whereby the treatment of nematodes with anti- necessary nucleotides, cofactors and bacteria and their hosts.
These bacteria infect not only 70% of offspring of uninfected females and infected males fail to biotics that are targeted at elimin- vitamins.
insects, but also the most abundant develop. Wolbachia are maternally inherited, being transferred ating the Wolbachia infection also Despite maternal inheritance in Interdomain lateral gene
animal phyla, including nematodes and through the egg cytoplasm. Therefore, these reproductive kills the host. This suggests that Wol- arthropods, arthropod-borne Wolbachia transfer
arthropods. phenotypes favouring Wolbachia-infected females increase bachia form an obligate mutualistic do not evolve with the host. Instead, the In 2001, Natsuko Kondo and
The arthropod-infecting Wolbachia exert unusual effects on the proliferation of Wolbachia-infected arthropods. Wolbachia symbiosis with filarial nematodes, bacteria are transmitted horizontally colleagues described a variant of a
host reproduction, including: (1) parthenogenesis, whereby are parasitic endosymbionts, since the interaction benefits since neither organism can survive and infections are lost, although the bean beetle, Callosobruchus chinensis,
infected virgin females produce infected female offspring, Wolbachia while exerting a negative effect on the host by without the other. The exact nature mechanisms are not understood. In where Wolbachia genes had moved
(2) male killing, whereby infected male embryos fail to limiting genetic exchange. However, a mutualistic role of the mutualistic interaction is not contrast, filarial nematodes and into the insect chromosome. This
develop, (3) feminization, whereby genetic males develop benefiting both organisms cannot be excluded. known, but it has been proposed Wolbachia evolve together, reflecting movement of DNA from an organism
176 microbiology today nov 08 microbiology today nov 08 177You can also read
