Introducing the Microbial Ecology of Changing Environments Collection

We are very pleased to be launching our Microbial Ecology in Changing Environments Collection, the product of a call for papers convened by PLOS ONE and our Guest Editors, Melissa Cregger and Stephanie Kivlin. The research in the Collection crosses disciplinary boundaries and represents a wide range of geographies, providing a snapshot of the diversity of research in contemporary microbial ecology. More articles will be added in due course, so please check back for updates!

Several articles highlighted in the Collection address the structure and dynamics of microbial communities in marine or aquatic environments. Three North American studies feature in the initial set of articles. Working in the Southern Californian Bight, Larkin and colleagues explored the effect of El Niño events on cyanobacterial populations [1]. Meanwhile, Vogel and colleagues found evidence for environmental and host-specific influences on microbial community structure on seagrass off the coast of Florida [2]. Finally, using a wetland mesocosm in Connecticut, Donato and co-workers performed an integrative study of microbial and plant responses to simulated chemical pollution [3].

The impact of natural disturbance on microbial communities was another theme that emerged in submissions to the Collection. In this first batch of articles, this is represented by the work of Eaton and colleagues, who examined how a major hurricane affected soil microbes in primary forests in Costa Rica [4].

The microbial ecology of manmade environments also features in the Collection. Maguvu and co-workers analysed the microbiome and physicochemical properties of drinking water production plants in South Africa, identifying significant variation in microbial community structure between facilities [5].

Last but not least, the Collection includes new research on the relationships between microbial communities living in dynamic environments within host organisms. Working in the UK, Garber and colleagues examined the effect of abrupt dietary changes in ponies on gut microbiota, with important implications for animal management [6].

The research in the Collection provides valuable insights into the mechanisms and consequences of microbial interactions with dynamic environments, and highlights the broad range of systems in which scientists are actively engaged in elucidating these phenomena.

References

  1. Larkin AA, Moreno AR, Fagan AJ, Fowlds A, Ruiz A, Martiny AC (2020) Persistent El Niño driven shifts in marine cyanobacteria populations. PLoS ONE 15(9): e0238405. https://doi.org/10.1371/journal.pone.0238405
  2. Vogel MA, Mason OU, Miller TE (2020) Host and environmental determinants of microbial community structure in the marine phyllosphere. PLoS ONE 15(7): e0235441. https://doi.org/10.1371/journal.pone.0235441
  3. Donato M, Johnson O, Steven B, Lawrence BA (2020) Nitrogen enrichment stimulates wetland plant responses whereas salt amendments alter sediment microbial communities and biogeochemical responses. PLoS ONE 15(7): e0235225. https://doi.org/10.1371/journal.pone.0235225
  4. Eaton WD, McGee KM, Alderfer K, Jimenez AR, Hajibabaei M (2020) Increase in abundance and decrease in richness of soil microbes following Hurricane Otto in three primary forest types in the Northern Zone of Costa Rica. PLoS ONE 15(7): e0231187. https://doi.org/10.1371/journal.pone.0231187
  5. Maguvu TE, Bezuidenhout CC, Kritzinger R, Tsholo K, Plaatjie M, Molale-Tom LG, et al. (2020) Combining physicochemical properties and microbiome data to evaluate the water quality of South African drinking water production plants. PLoS ONE 15(8): e0237335. https://doi.org/10.1371/journal.pone.0237335
  6. Garber A, Hastie P, McGuinness D, Malarange P, Murray J-A (2020) Abrupt dietary changes between grass and hay alter faecal microbiota of ponies. PLoS ONE 15(8): e0237869. https://doi.org/10.1371/journal.pone.0237869

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It’s the little things- An interview with the Guest Editors of our Microbial Ecology of Changing Environments Call for Papers

PLOS ONE has an open Call for Papers on the Microbial Ecology of Changing Environments, with selected submissions to be featured in an upcoming Collection. We aim to highlight a range of interdisciplinary articles showcasing

It’s the little things- An interview with the Guest Editors of our Microbial Ecology of Changing Environments Call for Papers

PLOS ONE has an open Call for Papers on the Microbial Ecology of Changing Environments, with selected submissions to be featured in an upcoming Collection. We aim to highlight a range of interdisciplinary articles showcasing the diversity of systems, scales, interactions and applications in this dynamic field of research.

We spoke to the Guest Editors for this project, Melissa Cregger and Stephanie Kivlin, about what motivates their research and the challenges and opportunities faced by microbial ecologists.

 

What makes microbes so interesting?

MC: Microorganisms are everywhere and are important members of all of the ecosystems they inhabit. There are microorganisms in soils, oceans, lakes, and even within our bodies. Within all of these habitats they are performing really important functions. In lakes, oceans, and soils, microorganisms are key to moving nutrients around. Within our bodies, they aid in things like digestion and disease prevention.

SK: Microorganisms are fascinating in how genetically diverse and numerous they are. Microorganisms can be found in almost every habitat on Earth and are often the first to respond to environmental disturbance and global change. Thus, microorganisms likely hold the key to solving most of Earth’s problems as we face global climate change.

 

How is microbial ecology relevant to major environmental and societal issues like climate change and food security?

MC: Given how ubiquitous microorganisms are across the world, understanding how they function is key if we want to understand and mitigate the consequences of climatic change and if we want to grow food more sustainably and in marginal lands. For instance, if we can get a better understanding of microbial carbon cycling, we can potentially use biological carbon capture as a mitigation strategy to help combat rising levels of atmospheric carbon dioxide. Additionally, researchers around the world are trying to understand how plants interact with microbial communities in an effort to harness these microbes to increase food production and the ability of plants to withstand changing abiotic conditions.

SK: Microorganisms are the key for innovating nature-based solutions to climate change. For example, specific fungal symbionts of plants can be tailored to increase agricultural plant drought tolerance. Other microorganisms may be deployed to remediate oil spills or other man-made pollutants. Finally, engineering plant-microbial associations may lead to a larger terrestrial carbon sink to offset atmospheric CO2 concentrations, creating a negative feedback to climate change itself.

 

Tell us a bit about your own research and how it ties in with some of these issues.

MC:  A large portion of my research is focused on understanding how to use beneficial microbes to increase plant productivity and tolerance to drought, and also in understanding how these communities function in the soil environment with the ultimate goal of using them to enhance ecosystem stability. I am part of two large multi-disciplinary teams at Oak Ridge National Laboratory that are specifically focused on plant-microbe interactions in the potential biofuel feedstock, Populus. We are trying to characterize basic principles governing plant-microbe interactions in the hope of making Populus a better biofuel that can grow in marginal lands with limited input of fertilizer and water.

SK: Research in the Kivlin Lab aims to create distribution models for terrestrial microorganisms and their functions. Our current focus is on arbuscular mycorrhizal (AM) fungi, as these plant symbionts are the main providers of nutrients and drought tolerance to agricultural plants. We are interested in where these fungi are, the ecosystem-level carbon and nutrient cycling they promote and how sensitive these plant-fungal interactions may be to climate change. To address these questions, we both compile data on AM fungal distributions worldwide, but also examine plant-AM fungal interactions along altitudinal gradients that serve as a space for time substitution for climate change and in long-term climate change experiments.

 

How are technological advances opening up new opportunities in your field?

MC: Over the last 20 years there have been rapid advances in sequencing and molecular techniques that have enabled amazing opportunities in microbial and ecosystem ecology. We are finally able to identify unculturable microorganisms inhabiting diverse communities using next generation sequencing and are getting clues into their function using metagenomics, metatranscriptomics, proteomics, and metabolomics. Further, using these techniques, people are developing some new strategies to culture more microbes.

SK: It is increasingly clear that the genomics revolution has impacted microbial ecology. We now can link functional genetic potential to microorganisms in environmental microbiomes and understand how interactions among microorganisms and between microorganisms and plants control expression of these functional genes and the metabolites they code for.

 

How does microbial ecology benefit from interdisciplinary collaboration?

MC: Microbial communities are incredibly complex, therefore understanding their role in ecosystems really requires a systems biology approach. Because of this, having an interdisciplinary team to tackle questions at various scales is really important.

SK: Microbial ecology is inherently interdisciplinary. We collaborate with earth system modelers to scale microbial function from the organism to the globe and with geneticists to understand the genetic underpinnings of those functions. Without these collaborations, our field would be siloed to case-studies of microbial communities and lack the ability to develop first-principles theory across microbial communities and environments.

 

What are some of the biggest unsolved questions in microbial ecology?

MC: There are so many unsolved questions in microbial ecology that it is hard to just identify a few. We still have a limited understanding of how microbial communities fluctuate through time. How stable are they within ecosystems? Are organisms within communities functionally redundant? Does this redundancy aid in resilience of the community post disturbance? How do these communities respond to fluctuations in abiotic variables? I could really go on and on.

SK: Despite all of the vital roles that microorganisms provide in the environment, we still don’t understand (1) where microorganisms even are spatially and what abiotic and biotic processes control these distributions, or (2) how temporally dynamic microbial communities are both within and among plant growing seasons. Answering these fundamental questions will allow us to understand linkages between microbial communities and plant growth, microbial composition and ecosystem carbon and nutrient cycles, and allow us to effectively manipulate microbial consortia for societal gain in agricultural and bioremediation settings.

 

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From Penguins to Frogs: The new frontier of wildlife microbiomes

With recent technological advances in DNA sequencing investigating microbiomes from all areas of life has become possible as PLOS ONE Publication Assistant Maija Mallula finds out. With the advancement of DNA sequencing technology, our ability

Resisting Antibiotics: Some Bacteria Get By With a Little Help From Their Friends

burkholderia

Antibiotic resistance is often in the news, as it threatens the effectiveness of one of the foundations of modern medicine. Usually, the concern is about resistance that is inherent to the bacteria, or else develops in bacteria through genetic changes. A paper published today in PLOS ONE suggests another possibility.

In “Chemical communication of antibiotic resistance by a highly resistant subpopulation of bacterial cells,” authors Omar El-Halfawy and Miguel Valvano reveal that some species of bacteria may help others in surviving an antibiotic attack. In addition, they were able to provide insight into the mechanics of how the bacteria perform this action.

The study began with an observation of the bacterial species Burkholderia cenopecia, which typically grows in the soil but can infect people who have cystic fibrosis and those with compromised immune systems. The authors noted that a subpopulation of the species was more resistant to the antibiotic polymyxin B than other bacteria of the species. In other words, these resistant bacteria were more likely to survive after treatment with polymyxin B, and levels of antibiotics that killed the less resistant bacteria did not harm this (more resistant) subpopulation.

When the authors grew the more-resistant B. cenopecia with another strain of bacteria called Pseudomonas aeruginosa (a disease-causing bacterium that can co-exist with B. cenopecia), the P. aeruginosa were much more resistant to the antibiotic than when they grew in isolation.

Why might the P. aeruginosa be more resistant when they were in the presence of B. cenopecia?

The authors suspected that the B. cenopecia were releasing something into their environment that interfered with the action of the antibiotic, making it less potent. Experiments revealed that the bacteria were indeed secreting two proteins associated with increased antibiotic resistance: putrescine (named for its putrid odor!) and Ycel, a protein whose function was previously unknown.

cartoon 3

The large amounts of secreted putrescine blocked the antibiotics’ binding to the surface of the bacteria, and could make both B. cenopecia and P.aeruginosa more resistant to polymyxin B when grown together.

Ycel, on the other hand, was able to bind to the antibiotic directly, presumably decreasing its potency. Ycel is predicted to bind amphiphilic molecules (such as detergents, which  are attracted to both water and oil). Consistent with this prediction, the authors showed that Ycel had a protective effect against amphiphilic antibiotics and less of an effect against others.

These results have implications for combating the growing problem of antibiotic resistance. If we could prevent bacteria from making putrescine or Ycel, antibiotic treatments might be more effective, helping us eventually outflank resistance.

Citations: El-Halfawy OM, Valvano MA (2013) Chemical Communication of Antibiotic Resistance by a Highly Resistant Subpopulation of Bacterial Cells. PLoSONE 8(7): e68874. doi:10.1371/journal.pone.0068874

Bragonzi A, Farulla I, Paroni M, Twomey KB, Pirone L, et al. (2012) Modelling Co-Infection of the Cystic Fibrosis Lung by Pseudomonas aeruginosa and Burkholderia cenocepacia Reveals Influences on Biofilm Formation and Host Response. PLoS ONE 7(12): e52330. doi:10.1371/journal.pone.0052330

Images: Pseudomonas aeruginosa doi:10.1371/journal.pone.0066257

Opportunistic pathogens evolve mostly harmlessly in healthy humans

Staphylococcus_aureus_VISA_2

Humans interact with bacteria almost every minute of our lives. Of the millions of these interactions, only a handful result in disease, and some bacteria only cause infections under certain conditions. In a recent PLOS ONE study, researchers probe these healthy human-bacterial relations  in one particularly notorious pathogen as it spends the majority of its time in our bodies, doing no harm.

Staphylococcus aureus can cause endocarditis, toxic shock syndrome and other diseases, killing approximately 1 in 100,000 infected people in the US each year. Strains like MRSA have also evolved to carry multiple antibiotic resistance genes, making infections extremely difficult to treat. If human-bacterial interactions are to be described as a ‘genetic arms race’, it may be tempting to cast S. aureus as an enemy that carries every available genetic weapon.

Yet despite a few sporadic skirmishes, the majority of our interactions remain peaceful, as these bacteria thrive in healthy human hosts.  In fact, about a third of healthy adults carry S. aureus in our noses at some point in our lives.  In the article, researchers analyzed the genetic changes in S. aureus carried in such hosts by sequencing the genomes of 130 strains of S. aureus from the nasal passages of 13 healthy adults, five of whom carried strains of MRSA (which is often harmless when carried nasally). Despite the arms race metaphors, they found that S. aureus strains in healthy hosts are not incessantly beefing up their genetic arsenal of antibiotic resistance or pathogenesis genes.

They found bacterial genomes were changed by processes of ‘micro-mutation’, i.e.: small bits of genetic material being added or removed, or changes in a single letter in the genetic code. Large insertions and deletions (macro-mutation) were also common, as were changes caused by bacteria-infecting viruses or small, independently moving rings of DNA called plasmids. Overall, the constant changes in S. aureus genomes were geared toward keeping bacterial genomes healthy by clearing erroneous or harmful mutations. Only on rare occasions did these bacteria acquire distinctive surface proteins or an enterotoxin that could alter their pathogenic potential. In addition, their research also analyzed changes in specific genes used to assess bacterial diversity and relatedness, and developed a new method to detect transmission of bacterial strains among human carriers. Read the full study to learn more about these interesting results.

Many of the changes identified in this study may not directly increase the virulence of disease-causing S. aureus. However, previous work by these researchers demonstrated that mutations arising in bacteria carried by healthy hosts may play an important role in tipping the balance between human health and disease. Here, the authors begin to paint a picture of what these mutations are and how they may occur.

Citation: Golubchik T, Batty EM, Miller RR, Farr H, Young BC, et al. (2013) Within-Host Evolution of Staphylococcus aureus during Asymptomatic Carriage. PLoS ONE 8(5): e61319. doi:10.1371/journal.pone.0061319

Image: Scanning electron micrograph of S.aureus with increased resistance to vancomycin. Credit CDC/ Matthew J. Arduino, DRPH

 

PLOS ONE Goes to the Mile-High City for ASM 2013

Bacillus anthracis - three color

PLOS ONE is looking forward to connecting with our editors, authors, reviewers, and readers at the 113th General Meeting of the American Society for Microbiology in Denver, Colorado. Representing PLOS ONE will be Damian Pattinson, Executive Editor; Lindsay Kelley, Editorial Board Manager; Camron Assadi, Product Marketing Manager; and myself (Meg Byrne, Associate Editor).

PLOS ONE continues to publish many high-profile papers in microbiology. Some of the most highly cited articles published since 2011 include a genomic characterization of a deadly Escherichia coli strain; a “field guide” to more than 3000 isolates of methicillin-resistant Staphylococcus aureus found around the world; the genome sequence of a novel ammonia-oxidizing archaeon (a member of the recently discovered third domain of life); and an analysis of the lung microbiomes in smokers with chronic obstructive pulmonary disease, smokers without COPD, and non-smokers.

In the last month, a number of publications have caught our readers’ eyes.  These include an article showing that a breast-milk protein can help fight antibiotic-resistant bacteria; a report of a new antibiotic developed from a bacteria-killing virus; a super-phylogeny of the over 3000 bacterial and archaeal genomes that have been sequenced to date; and an analysis of the immune response to a bacterial lung infection in a 500-year-old mummy.

Come find us at the meeting: We’d love to hear your thoughts about PLOS and science publishing, in general. We’ll be at booth #350 from Sunday, May 19th through Tuesday, May 21st.

For authors: Let us show you your article level metrics (ALMs) and give you a special author t-shirt.  We can also show off one of our latest features, Relative Metrics (Beta), which allows you to compare your paper’s usage to the average usage of articles in related subject areas.

For prospective authors: Please come ask us any questions you have about publishing in PLOS ONE and the family of PLOS journals. We can enumerate the many advantages of publishing in our open access journals, including free readership rights, reuse and remixing rights, unrestricted copyright, automatic posting of the article, and machine accessibility of the published article.

For PLOS ONE academic editors: We are looking forward to seeing you at our Editorial Board Reception on Monday May 20th from 5:30 to 7:30 PM at the Hyatt Regency.  We would love to fill you in on our plans for the future, get your feedback, and say a huge “Thank you!” It’s also a great opportunity to meet other academic editors. Please contact Lindsay Kelley or Camron Assadi for further information.

Also, PLOS Biology is looking forward to catching up with their academic editors at a “Meet the Editors” event on Sunday May 19th between 12:30 and 2:30 PM at the PLOS Booth.

We’re looking forward to seeing many microbiologists in Denver and discussing the small but mighty microbe.

Image

Bacillus anthracis with the cell wall labelled red, the division septa labelled green, and the DNA labelled blue (Schuch et al. PLOS ONE 2013).

References

Blainey PC, Mosier AC, Potanina A, Francis CA, Quake SR (2011) Genome of a Low-Salinity Ammonia-Oxidizing Archaeon Determined by Single-Cell and Metagenomic Analysis. PLoS ONE 6(2): e16626. doi:10.1371/journal.pone.0016626

Corthals A, Koller A, Martin DW, Rieger R, Chen EI, et al. (2012) Detecting the Immune System Response of a 500 Year-Old Inca Mummy. PLoS ONE 7(7): e41244. doi:10.1371/journal.pone.0041244

Erb-Downward JR, Thompson DL, Han MK, Freeman CM, McCloskey L, et al. (2011) Analysis of the Lung Microbiome in the “Healthy” Smoker and in COPD. PLoS ONE 6(2): e16384. doi:10.1371/journal.pone.0016384

Lang JM, Darling AE, Eisen JA (2013) Phylogeny of Bacterial and Archaeal Genomes Using Conserved Genes: Supertrees and Supermatrices. PLoS ONE 8(4): e62510. doi:10.1371/journal.pone.0062510

Marks LR, Clementi EA, Hakansson AP (2013) Sensitization of Staphylococcus aureus to Methicillin and Other Antibiotics In Vitro and In Vivo in the Presence of HAMLET. PLoS ONE 8(5): e63158. doi:10.1371/journal.pone.0063158

Mellmann A, Harmsen D, Cummings CA, Zentz EB, Leopold SR, et al. (2011) Prospective Genomic Characterization of the German Enterohemorrhagic Escherichia coli O104:H4 Outbreak by Rapid Next Generation Sequencing Technology. PLoS ONE 6(7): e22751. doi:10.1371/journal.pone.0022751

Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, et al. (2011) A Field Guide to Pandemic, Epidemic and Sporadic Clones of Methicillin-Resistant Staphylococcus aureus. PLoS ONE 6(4): e17936. doi:10.1371/journal.pone.0017936

Schuch R, Pelzek AJ, Raz A, Euler CW, Ryan PA, et al. (2013) Use of a Bacteriophage Lysin to Identify a Novel Target for Antimicrobial Development. PLoS ONE 8(4): e60754. doi:10.1371/journal.pone.0060754