29 September 2021
Benchmarking microbial growth rate predictions from metagenomes
Citation: Long AM, Hou S, Ignacio-Espinoza JC, Fuhrman JA. (2021). Benchmarking microbial growth rate predictions from metagenomes. The ISME Journal 15:183–195.
 
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by Sarah Preheim

I regularly remind myself and my students that you will always come up with an answer when you apply some analysis to your data, but how do you know whether the answer you get is right? This can be particularly challenging when studying uncultured microorganisms in the environment because it isn't always clear what the right controls are. Work by Long and his colleagues sought to answer this question for techniques that have become increasingly popular to use to measure microbial growth characteristics of uncultured microorganisms using metagenomic data. Measurements or estimates of microbial growth can reveal the important role these tiny creatures play in the ecosystem. Yet, a majority of environmental microorganisms can't be cultured to determine their maximum growth rate or identify how changing environmental conditions influences their growth. Even for organisms in culture, it is difficult to determine the actual growth rates that microorganisms experience under in situ environmental conditions because environmental conditions are difficult to recreate in the laboratory. Thus, techniques to estimate these parameters from metagenomic data have been developed, either through inherent genome characteristics (i.e. codon usage bias, CUB) or the distribution of reads or observations over the genome (e.g. peak-to-trough ratio, PTR). While these techniques were tested and validated with cultured microorganisms, the effectiveness of these techniques for uncultured microorganisms using shotgun metagenomics had not been thoroughly validated.

The work by Long and colleagues more rigorously tests the ability of a variety of techniques to estimate these growth characteristics using methodology typical for environmental studies. By applying these techniques within experimental incubations of natural seawater, filtered to remove grazers and viruses so that changes in cell number better approximate growth, they compared the observed growth to growth estimated by CUB or PTR with metagenomics. CUB estimates were significantly correlated with maximum growth, suggesting they are a reasonable measure of the maximum growth rate for a diverse range of environmental marine microbes. However, PTR estimates were not well correlated to growth for the entire community and only showed positive correlations with growth for a subset of the community. Interestingly, Gammaproteobacteria was one taxonomic group for which this technique worked well. Thus, this work better defines the limitations of these approaches and highlights the importance of continuing to ask this basic question of your analysis- how do you know whether the answer you get is right?

About the author Andrew M. Long: My academic journey started at Texas A&M, where my eyes were opened to the microbial world through a spectacular first year biology course taught by Dr. Michael Manson. His lectures got me hooked on the fascinating world of life at low Reynold’s numbers and the semester-long laboratory that consisted of generating and then characterizing mutants of E. coli gave me my first glimpse into detailed experimentation. In addition, my undergraduate research was on bacterial-mediated cotton boll rot with Dr. Alois Bell at the USDA-ARS in College Station, TX. I kept with the farm theme and studied anammox and denitrification (both fungal and bacterial) in agricultural soils during my masters at UNCW with Dr. Bongkeun Song. After spending a year as a high throughput sequencing technician, I got the academic itch back. I then proceeded to study algal viruses and cyanophages in freshwater environments during my PhD at the University of Toronto with Dr. Steven Short. More recently, I’ve ventured into marine microbial ecology, looking at the ‘omic signatures of bacterial growth and the production of viruses with Dr. Jed Fuhrman at USC. I am continuing my work in marine systems here in our lab at LSU, studying the effects of viruses on oxygen minimum zones and hydrothermal vent ecologies. Broadly speaking, I am interested in deciphering how the interactions of microbes across multiple trophic levels modulate global processes. 

29 September 2021
Depth-discrete metagenomics reveals the roles of microbes in biogeochemical cycling in the tropical freshwater Lake Tanganyika
Citation: Tran PQ, Bachand SC, McIntyre PB, Kraemer BM, Vadeboncoeur Y, Kimirei IA, Tamatamah R, McMahon KD, Anantharaman K. (2021) Depth-discrete metagenomics reveals the roles of microbes in biogeochemical cycling in the tropical freshwater Lake Tanganyika. The ISME Journal 15:1971–1986.
 
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by Sarah Preheim

Lake Tanganyika is a unique ecosystem in many ways and the work by Tran and colleagues provides an in-depth analysis into the diversity and function of the microorganisms that inhabit it. Lake Tanganyika is the second largest freshwater by volume in the world, harboring 16% of the Earth's freshwater. Microbial processes within this ecosystem have a major impact on local biogeochemical cycles, such as the generation and consumption of substantial amounts of methane (23 Tg) that collect below the depth where oxygen concentrations become undetectable. Freshwater tropical lakes are typically nitrogen-limited, so nitrogen cycling can influence the food web and overall productivity of the lake. By conducting shotgun metagenomic sequencing of 24 samples from depths up to 1200 m and metagenomic binning to reconstruct 523 metagenome assembled genomes, the authors were able to identify a number of unique and unexpected microorganisms and their associated biogeochemical functions.

Among their discoveries is a novel species (Candidatus Tanganyikabacteria) most closely related to the non-photosynthetic Cyanobacteria-like Sericytochromatia. Sericytochromatia genomes had not been reconstructed and functionally described from the water column of freshwater lakes before. They also found that Lake Tanganyika had a large number of unique reconstructed genomes compared to those found in the deepest freshwater lake in the world, Lake Baikal. The microorganisms unique to Lake Tanganyika are likely related to the differences in geochemical parameters between the lakes, as Lake Baikal is oxygenated at depth and is seasonally ice-covered. Nitrogen-fixation was not found in any Cyanobacterial genomes, but within a diversity of organisms that were more similar to those of a stratified, humic lake. Denitrification potential was found in reconstructed genomes at a similar relative abundance at all depths. Bacteria capable of anammox, a process that also result in a loss of fixed nitrogen from this system, were also found throughout the lake. As climate change is expected to increase the number of stratified, anoxic lakes globally, this study provides an insight into the distribution of biogeochemical functions mediated by microorganisms that have important ecosystem functions within these systems.

About the author:  Patricia Tran is a PhD Candidate in Freshwater and Marine Sciences at the University of Wisconsin-Madison (WI, USA) where she is co-advised by Dr. Katherine (Trina) McMahon and Dr. Karthik Anantharaman. She studies microbial ecology, microbial metabolism and biogeochemistry in freshwater lakes. She is particularly interested in anoxic and spatio-temporally dynamic ecosystems.

30 August 2021

Bacterial controlled mitigation of dysbiosis in a seaweed disease
Citation: Li J, Majzoub ME, Marzinelli EM, Dai Z, Thomas T, & Egan S. (2021). Bacterial controlled mitigation of dysbiosis in a seaweed disease. ISME J (2021). https://doi.org/10.1038/s41396-021-01070-1.
 
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by Jillian Petersen

Since the work of microbiologists such as Robert Koch et al. more than 100 years ago, we’ve known that some bacteria cause diseases. We are now entering an exciting new era where we are beginning to recognize that some bacteria could be used to prevent or even cure diseases. Helpful bacteria employed in this way are referred to as ‘probiotics’, usually in the context of applying live microorganisms to improve human health.

A recent study by Jiasui Li et al, in a team led by Suhelen Egan at the Centre for Marine Science and Innovation, University of New South Wales, contributes to the emerging field of probiotics for application in environments such as the oceans, to improve or maintain marine organism health. The disease in question is bleaching of the red macroalga Delisea pulchra, which causes the algae to lose photosynthetic pigments. Like numerous diseases of marine organisms, D. pulchra bleaching is associated with the presence of particular bacteria that can trigger the disease, in this case some Phaeobacter, Aquinimarina, Agarivorans, and Alteromonas species.

The team used a diffusion-based plate agar bioassay to assess the potential of hundreds of strains isolated from healthy seaweeds to inhibit growth of these potential pathogens. One strain was of particular interest – Phaeobacter sp. BS5 (not to be confused with the disease-triggering Phaeobacter strains!), which inhibited the growth of several pathogens. Likewise, adding Phaeobacter sp. BS5 to seaweeds in aquaria had a significant protective effect when the pathogen Aquinimarina sp. AD1 was also added. Considering the inhibitory growth effects of Phaeobacter sp. BS5 on the pathogens in plate assays, the team expected a negative correlation between the relative abundance of these two organisms on the experimental seaweeds – indicating that the protective strain directly inhibits pathogen growth on the seaweeds as it did in the lab. Surprisingly, this was not the case. Instead, 16S rRNA gene amplicon assays revealed a general shift in microbial community composition in the presence of the pathogen, which did not take place when pathogen and Phaeobacter BS5 were both applied. The protective effect might therefore be due to indirect interactions, for example, through Phaeobacter sp. BS5 strengthening the resistance of the native microbiome to disturbance, rather than direct interactions between probiotic and pathogen.

This result is intriguing because it expands the range of microbes that could potentially be harnessed as probiotics. Even strains that do not directly affect pathogen growth could still protect against disease through interactions with other members of the native microbiome. This study also provides another fascinating example of how even closely-related microbial strains have the potential to cause or prevent disease, which are arguably diabolically opposite functional roles. The taxonomic groups studied here including Phaeobacter, Vibrio, and Pseudoalteromonas, are widespread and diverse associates of marine organisms, and despite sharing a (genus) name, contain members that might provide the clues to both the causes and the cures of a range of diseases.

About the first author: Jiasui Li studied Chinese Pharmacy completing a BSc and MSc from Chengdu University of Traditional Chinese Medicine, China. Her MSc thesis was on characterising fungal pathogens causing root-rot disease in a cultivated Chinese herb, where she developed a strong interest in microbial ecology. She is now doing her PhD with Dr Suhelen Egan (senior author) at the University of New South Wales, Sydney Australia, where her project focuses on host-bacterial interactions and biocontrol for seaweed diseases.

Check out the paper for the full story.

30 August 2021

Coming together—symbiont acquisition and early development in deep-sea bathymodioline mussels
Citation: Franke M, Geier B, Hammel JU, Dubilier N, Leisch N. (2021). Coming together—symbiont acquisition and early development in deep-sea bathymodioline mussels. Proceedings of the Royal Society B, volume 288, issue 1957; DOI: 10.1098/rspb.2021.1044.
 
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by Jillian Petersen

We all want to ensure our kids are equipped to survive in the world - provide them with a high-quality education, solid work ethic, self-confidence, but how often do we think about equipping them with the right microbes? Providing offspring with the microbial partners that will ensure proper development and long-term health is a central challenge, but we know very little about how most organisms overcome this challenge because it is so difficult to observe in nature. Understanding symbiont transmission between host generations is particularly challenging in remote locations such as at deep-sea hydrothermal vents and cold seeps, but is important because entire ecosystems in these habitats rely on invertebrates such as Bathymodiolus mussels finding and coming together with particular species of chemosynthetic bacteria that provide them with nutrition.

Maximilian Franke and a team of colleagues led by Nikolaus Leisch and Nicole Dubilier from the Max Planck Institute for Marine Microbiology have just provided the most spectacularly detailed insights so far into symbiont transmission in Bathymodiolus mussels. They collected very early developmental stages of several Bathymodiolus species from the Atlantic Ocean and Gulf of Mexico, the smallest of which were symbiont-free pediveliger larvae, less than 400 um in length. The team overlaid a very impressive range of imaging methods including histology, electron microscopy, DOPE-FISH and synchrotron radiation-based micro-computed tomography, to follow the very first stages of symbiont acquisition and development. Symbionts were never present in pediveligers, which is the final free-swimming developmental stage, but were found in all larvae undergoing metamorphosis after settling on the sea floor. Symbionts colonized all epithelial tissues of the developing mussels, in contrast to the adults, where colonization is restricted to the gill epithelia. The range of morphological changes triggered in the animal hosts after symbiont colonization is remarkable, ranging from the cellular level, including loss of cilia and microvilli from the cells colonized by symbionts, to changes in the length and complexity of the digestive tract. Bathymodiolus and its intracellular chemosynthetic symbionts are a beautiful example of coordinated development between animals and microbes that must involve intricate and highly specific mechanisms of inter-domain communication.

One interesting finding was the lack of ‘intermediate’ stages between initial colonization by a few symbiont cells, and fully colonized individuals. This could have been missed due to under sampling, however, it may also be that once initiated, the symbiosis rapidly becomes fully established. Even hydrothermal vent mussels seem to have efficient mechanisms to ensure their offspring find the symbiotic bacteria they need for their survival.

About the authors: Maximilian Frankeis a PhD student at the Max Planck Institute for Marine Microbiology in Bremen. His research interests are symbiotic associations between eukaryotes and prokaryotes. In particular, he is interested in the effects of bacterial colonization on host morphology and ecology.

Niko Leisch is a project leader at the Max Planck Institute for Marine Microbiology. As an organismal scientist he is fascinated by host-microbe interactions. His research focusses on how bacteria are integrated into the host's life-cycle and into the host's tissue, cells and organelles.

Check out the incredibly beautiful images in the original paper.
28 June 2021

Specific modulation of the root immune system by a community of commensal bacteria
Citation: Teixeira PJPL, Colaianni NR, Law, TF, Conway JM, Gilbert S, LiH, Salas-González I, Panda D, Del Risco NM, Finkel OM, Castrillo G, Mieczkowski P, Jones CD, Dangl JL. (2021). Specific modulation of the root immune system by a community of commensal bacteria. Proceedings of the National Academy of Sciences Apr 2021, 118 (16) e2100678118; DOI: 10.1073/pnas.2100678118.
 
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by Damien Gayrard

Plant-associated commensal bacteria represent a subset of those in the bulk soil. This is at least partly due to the sophisticated innate immune system that plants have evolved and allow them to select between beneficial, neutral, or harmful microbes. The MAMP-triggered immunity (MTI) is the first layer of that defence system. It is based on pattern recognition receptors (PRRs) detecting epitopes such as flg22, a 22-amino acids epitope found in the bacterial flagellum. MTI has been thoroughly studied in the context of interaction with pathogens. To interfere with plant innate immunity, pathogens have evolved host-specialised effector proteins often secreted by TSS3 (Type 3 Secretion System). Similar immunomodulation has previously been described by commensal strains but remains poorly understood in the context of community assembly.

Teixeira et al. investigated the modulation of Arabidopsis flg22-triggered immune response by a bacterial synthetic community (SynCom) composed of 35 representative commensals. While flg22 treatment induced a transcriptomic response of MTI marker genes both by control plants and plants inoculated with heat-killed bacteria, it was clearly suppressed by the plants inoculated with the living SynCom. Inoculated plants showed a specific transcriptomic pattern and flg22 did not affect assembly community composition. Hence, SymCom assembly actively interferes with flg22-driven MTI. Monoassociations showed that even if MTI suppression is the SynCom dominant trait, taken individually the strains can have inducer, neutral or suppressor effects on the plant response. Ten out of the 35 members of the SynCom were shown to be robust suppressors. Interestingly, the same robust suppressors were also the best root colonisers and were enriched into the endospheric compartment when the non-suppressors were not. Colonisation assays concluded that suppressor strains can enhance root colonisation capacities of other commensals. Thus, strains possessing immunomodulatory activity have a significant role in plant microbiota composition. Finally, the team investigated the mechanisms behind the robust suppression of the plant immune response by Dyella japonica MF79. Whereas its TSS3 was dispensable for the suppression ability, a forward genetic approach identified that a TSS2 (Type 2 Secretion System) was required for the suppression of MTI. No other genes were identified, thus implying that the suppression depends on the extracellular secretion of multiple compounds.

These findings suggest that modulation of host immune system is a widespread trait among root-associated bacteria. The presence of suppressor strains also benefiting to the non-suppressors. That low degree of specialisation is hypothesised to be caused by redundant immunosuppressive mechanisms acquired by the different commensals through evolution. Nonetheless, Teixeira et al. yielded highly valuable transcriptomic data that points up a core set of evolutionary conserved defence-related genes that are manipulated by commensal bacteria. These genes are promising candidates as key regulators of the plant immune response to bacteria colonisation and might play a key role in root microbiota homoeostasis.

About the first author: Paulo J. P. L. Teixeira received his PhD in Genetics and Molecular Biology from the University of Campinas (Unicamp) in 2013. He obtained a grant from the Pew Scholars Program in the Biomedical Sciences. He continued his research at the University of North Carolina, first at Jeff Dangl’s lab for his postdoctoral project and then as a researcher of the Howard Hughes Medical Institute (HHMI). He is now Assistant Professor at the University of Sao Paulo where he leads his own group investigating plant-microbe interactions.

21 June 2021
Microbial hitchhiking: how Streptomyces spores are transported by motile soil bacteria
Citation: Muok AR, Claessen D, Briegel A. (2021). Microbial hitchhiking: how Streptomyces spores are transported by motile soil bacteria. ISME J (2021). doi.org/10.1038/s41396-021-00952-8.
 
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by Laura Lehtovirta-Morley

Streptomyces are ubiquitous, non-motile bacteria in soils and perhaps best known for their antibiotic-producing properties. Soils harbour a very diverse microbial community, but until now, it has been unclear how non-motile microorganisms disperse through soils. Dr Alise Muok and Prof Ariane Briegel from Leiden University recently reported a fascinating discovery that Streptomyces spores can be transported by both gram-positive and gram-negative motile soil bacteria. Using several strains of Streptomyces as their model organisms, they demonstrated that Streptomyces spores adhere to the flagella of motile bacteria, allowing them to “hitchhike”. This ability is conserved in several species of Streptomyces and it is likely that their common ancestor, from 200 million years ago, was able to hitchhike too. There is an elegant mechanism enabling the transport. In most Streptomyces species, the spore coat contains a specific proteins called rodlins, which facilitate the attachment of the spores to the flagella. Streptomyces spores co-inoculated with the motile bacteria, B. subtilis, were also preferentially transported towards plant roots. This provides an interesting insight into how the plant rhizosphere microbiome may be formed.

Streptomyces have promising plant growth promoting and pathogen suppressing traits, and this work therefore has potential agricultural importance for crop production. It is also remarkable that the Streptomyces spores were able travel over a scale of centimetres. This work raises interesting questions on how common microbial hitchhiking is in soils, and whether there are other non-motile soil microorganisms which use a similar mechanism to disperse in soils.

About the authors: Dr Alise Muok is a Postdoctoral Research Associate at Leiden University. Her research centres on bacterial chemotaxis.

Prof Ariane Briegel is Professor of Ultrastructural Biology at Leiden University and a Co-director at the Netherlands Centre for Electron Nanoscopy. Her research focuses on bacterial chemotaxis and electron cryotomography.

15 June 2021

Nitrate is the new oxygen: anaerobic endosymbiont provides energy for its ciliate host through denitrification

Citation: Graf JS, Schorn S, Kitzinger K, et al. (2021) Anaerobic endosymbiont generates energy for ciliate host by denitrification. Nature 591: 445–450.
 
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by Laura Lehtovirta-Morley


The evolution of mitochondria conferred us and our early eukaryotic ancestors with the ability to breathe oxygen. However, amazingly little is known about the ability of eukaryotes to use electron acceptors other than oxygen for respiration. Dr Jon Graf, Dr Jana Milucka and colleagues at Max Planck Institute Bremen discovered a ciliate with a novel anaerobic endosymbiont which can respire nitrate instead of oxygen. The endosymbiont, ‘Candidatus Azoamicus ciliaticola’, was found in the anoxic, nitrate-rich zone in Lake Zug, Switzerland and yields energy for its eukaryotic host through denitrification. ‘Ca. A. ciliaticola’ has an extremely small, streamlined genome of 0.29 Mb, which encodes for a complete denitrification pathway and an ATP-generating electron transport chain. Remarkably, terminal oxidases were missing in both the endosymbiont and the host, suggesting that this ciliate is obligately, rather than facultatively, anaerobic. The host ciliate also lacks typical mitochondria which power ATP synthesis in most eukaryotic cells. In addition, the ciliate exhibited negative aerotaxis, consistent with the anaerobic lifestyle.

Ca. A. ciliaticola’ belongs to the gammaproteobacteria. Although ‘Ca. A. ciliaticola’ shares a rather similar function with mitochondria, the partnership between the host ciliate and its endosymbiont was established through a separate, more recent endosymbiotic event. Given the great diversity in metabolism and electron acceptors in prokaryotes, this study raises an exciting possibility that there may be other, as-yet undiscovered electron acceptors eukaryotes can use for respiration.


About the authors :

Dr Jana Milucka is a Group Leader in MPI for Marine Microbiology in Bremen. Her research interests span microbiology of methane and nitrogen cycling, anaerobic microbial metabolism and microbial symbioses.

 

Dr Jon Graf is a Postdoctoral Research Associate in MPI for Marine Microbiology in Bremen. His research focuses on biogeochemical cycling of methane and nitrogen in aquatic ecosystems.

 

31 May 2021
Host reproductive cycle influences the pouch microbiota of wild southern hairy-nosed wombats (Lasiorhinus latifrons)
Citation: Weiss S, Taggart D, Smith I, Helgen KM, Eisenhofer R. (2021) Host reproductive cycle influences the pouch microbiota of wild southern hairy-nosed wombats (Lasiorhinus latifrons). Animal Microbiome volume 3, Article number: 13 (2021).
 
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Marsupials are a group of mammals that we share a common ancestor with ~160 million years ago. A key taxonomic feature of marsupials is their early birth (1-6 weeks) followed by further development of the joey (young) in a pouch. See this cool video showcasing the epic journey joeys must make to reach their safety of their mother’s pouch. Being born young and without an immune system in a microbially rich world is challenging, and some known mechanisms for protecting the vulnerable joey include the transfer of antibodies and immune cells through milk, and the secretion of antimicrobial peptides into the pouch. However, little is known about the microbiology of the pouch – are there microbes present, and if so, are they influenced by the host’s reproductive status?

To fill this knowledge gap, we caught and sampled the pouch and other body sites from 26 wild female southern hairy-nosed wombats in South Australia (including both reproductively active females and subadults). We determined that there were indeed microbes present in the wombat pouch by using qPCR of the 16S rRNA gene and comparing 16S rRNA gene abundance to negative controls (sampling and extraction blanks). Next, using 16S rRNA gene sequencing we found that microbial composition of reproductively mature wombat pouches was distinct to that of other sample types, including subadult pouch samples, which resembled skin samples. Additionally, the number of amplicon sequence variants (ASVs) was drastically lower in reproductively active female pouches (mean 19) compared to subadult pouches (mean 941). Five microbial genera accounted for >90% of the microbial community in reproductively active pouches, and three of the five most abundant ASVs in these samples had closest BLAST matches to 16S rRNA gene sequences previously isolated from tammar wallaby pouches (another marsupial species).

Overall, our findings indicate that there appears to be a high degree of host filtering for what types of microbes can live in the pouch of reproductively active wombats. For the microbes that can survive in the pouch, how they do so, and what functions they possess remain to be discovered. The similarity of some of these wombat pouch microbes to microbes found in another marsupial species could indicate some degree co-speciation between host and pouch microbes. One possibility is that these pouch microbes could be beneficial to the host by occupying space and deterring pathogenic microbes from taking residence in the pouch. There is much still to learn about how microbes influence the evolution and ecology of Australia’s unique marsupials.


About the senior author: Raphael Eisenhofer received his PhD in paleomicrobiology in 2018 from the University of Adelaide. Since then, he has been a postdoc under the Centre of Excellence for Australian Biodiversity and Heritage, where he has focused on studying the microbial communities that inhabit Australia’s distinct native mammals.

 

14 May 2021

A genomic view of the microbiome of coral reef demosponges
Citation: Robbins SJ, Song W, Engelberts JP et al. A genomic view of the microbiome of coral reef demosponges. ISME J (2021). doi.org/10.1038/s41396-020-00876-9.
 
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Marine sponges are important for the health of coral reefs because of their role in the so-called “Sponge-Loop.” The crux of the Sponge Loop is that while coral reefs are one of the most productive ecosystems on earth, they are often referred to as “marine deserts” because ambient nutrient concentrations are low. Nutrient retention, then, is critical. Sponges filter out large quantities of organic matter released into the water column by other organisms living on the reef and convert it into sponge tissue. Their cells are then shed into the water column where they can be eaten by detritovores and the organic matter recycled back into the food chain, keeping these nutrients locked within the reef.

Tropical sponges, like most animals, host a variety of microbial symbionts (bacteria and archaea). These symbionts can make up to ~35% of the sponge’s total biomass and are thought to carry out a range of processes that are important for maintaining sponge health. For example, sponge symbionts are thought to provide the sponge with vitamins, remove waste ammonia, and potentially participate in the sponge loop by transforming components of dissolved organic matter. However, the majority of symbiont lineages found in tropical marine sponges remain largely uncharacterised, hampering our ability to identify core features of sponge symbionts, those that underpin the relationship between the host and its microbes.

To address this, we undertook an analysis of ~1200 metagenome-assembled genomes (MAGs) derived from seven marine sponge species and spanning 25 microbial phyla, allowing us to map functions thought to be important for sponge-microbe symbiosis across the vast majority of microbial taxa commonly found in marine sponges. This allowed us to identify specific functional guilds for the transformation of sugars common in coral reef dissolve organic matter, suggesting that microbes play a role in the Sponge Loop. We also show that the Thaumarchaeota are a keystone taxon for ammonia oxidation, and that many genes thought to be critical for maintaining sponge symbiosis (e.g. euk-repeat proteins) are not universally distributed among sponge symbionts, requiring some as-yet unknown mechanism in these lineages. Finally, we provide evidence that many of the genes thought to underpin sponge-microbe symbiosis, like the glycosyls hydrolases for transforming reef DOM, eukaryote-like proteins for evading the host immune system, and CRISPR and restriction-modification system genes for fending off viral infection, have been laterally transferred between disparate microbial lineages. Taken together, these data illustrate how evolutionary processes have partitioned ecological functions across sponge symbiont lineages, allowing them to occupy or share specific niches and live symbiotically with their sponge hosts.

About the first author: Steven Robbins received his PhD in 2015 from the University of Queensland, where he studied microbial metabolism in deep subsurface coal seams and the effects of hydrofracture stimulation on these communities with Dr. Gene Tyson. His postdoctoral work with the Great Barrier Reef Foundation’s ReFuGe2020 Consortium involved the integration of genomic data for several species of coral, as well as their Symbiodiniaceae and prokaryotic communities in order to clarify their individual roles within the coral holobiont. Following this, he joined Nicole Webster’s group at Australian Centre for Ecogenomics and the Australian Institute for Marine science to study the mechanisms underpinning sponge-microbe symbiosis. He now works with the Australian Integrated Marine Observing System working group to describe how changes in pelagic coral reef microbial communities reflect reef health.

14 May 2021

Continuous pre- and post-transplant exposure to a disease-associated gut microbiome promotes hyper-acute graft-versus-host disease in wild-type mice
Citation: Bowerman KL, Varelias A, Lachner N, Kuns RD, Hill GR, Hugenholtz P. (2020) Continuous pre- and post-transplant exposure to a disease-associated gut microbiome promotes hyper-acute graft-versus-host disease in wild-type mice. Gut Microbes, 1-17. doi.org/10.1080/19490976.2019.1705729.
 
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Graft-versus-host disease (GVHD) is a serious complication of hematopoietic stem cell transplantation occurring in 30-50% of cases. The gut microbiome has been observed to fluctuate both before and during the development of GVHD, creating a need to investigate whether there is a critical period during which the gut community composition can critically influence disease development. To investigate the contribution of the gut microbiome at different timepoints around the induction of GVHD, a team from the University of Queensland and QIMR Berghofer Medical Research Institute employed a mouse model system involving cohousing different strains of mice, with known divergent gut microbiomes, before and after stem cell transplant. They found that priming wild-type mice by cohousing them with a highly GVHD susceptible mouse strain prior to transplant did not affect disease progression, however, if cohoused after transplant, accelerated disease was observed. When wild-type mice were cohoused both before and after transplant, the effect of priming and post-transplant exacerbation were additive, resulting in a greater acceleration of disease beyond that seen with cohousing after transplant alone. Metagenomic analysis of the microbiome revealed pre-transplant cohousing was associated with the transfer of specific species within two as-yet-uncultured genera of the bacterial family Muribaculaceae; CAG-485 and CAG-873. Post-transplant, the authors observed GVHD-associated blooms of Enterobacteriaceae members Escherichia coli and Enterobacter hormaechei subsp. steigerwaltii, and a hyper-acute GVHD gut microbiome distinct from that associated with delayed-onset disease (>10 days post-transplant). These results clarify the importance of the peri-transplant microbiome in the susceptibility to acute GVHD post-transplant and demonstrate the species-specific nature of this association.

About the first author: Kate Bowerman received her PhD in Microbiology from the University of Queensland, Australia, in 2016. Her current research seeks to understand how microorganisms function in their environment and how they evolve over time to develop new capabilities using metagenomic techniques that permit the study of organisms not readily cultured within the laboratory.

26 April 2021

Contrasting patterns of microbial dominance in the Arabidopsis thaliana phyllosphere
Citation: Lundberg DS, de Pedro Jové R, Pramoj Na Ayutthaya P, Karasov TL, Shalev O, Poersch K, Ding W, Bollmann-Giolai A, Bezrukov I, and Weigel, D.  Contrasting Patterns of Microbial Dominance in the Arabidopsis Thaliana Phyllosphere. BioRxiv https://doi.org/10.1101/2021.04.06.438366.
 
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by Tatsuya Noborti

Aboveground organs of plants, or the phyllosphere, represent open and fluctuating habitats for microbes originating from various sources, such as soil, seeds, and from neighboring plants transferred via air, rain, insects, or other means. To date, the strain-level understanding of phyllosphere microbiome membership is limited, and best studied in the genus Pseudomonas. To better understand the ecology and host specificity in the phyllosphere microbiome, Lundberg et al. turned to another abundant yet less understood genus, Sphingomonas. The authors employed genomic techniques to analyze leaves of wild Arabidopsis thaliana and neighboring other plant species in spring, when A. thaliana plants were flourishing, and late summer, when there was no living A. thaliana. Amplicon sequencing of 16S rRNA genes revealed that both Sphingomonas and Pseudomonas dominated the leaf microbiome and were common endophytically, but Sphingomonas colonized more consistently in different seasons and had a broader host range than Pseudomonas. The authors established a genome-sequenced culture collection of endophytic Sphingomonas, which allowed for in-depth genome analyses at the strain level. The analysis revealed that Sphingomonas genomes are more diverse than Pseudomonas, and 16S rRNA information falls short in comprehending the diversity of plant-associated Sphingomonas. The authors also devised a cost-efficient metagenome approach in which Sphingomonas or Pseudomonas were enriched using cultivation on selective media before sequencing. The metagenome data showed that the most abundant strains of Sphingomonas and Pseudomonas in plants were not well represented in the soil, whereas some strains were shared between different plant species and, in some cases, between different seasons. These results suggest that leaf-to-leaf transmission may be a major source of these strains to the next generation. Overall, this study demonstrates the importance of strain-level analyses of the plant microbiome, and reveals shared and contrasting modes of interactions between leaves and dominant bacterial species in the phyllosphere.

About the first author: Derek S. Lundberg received his PhD in 2014 at the University of North Carolina at Chapel Hill, USA. There, in the lab of Jeff Dangl, he studied the Arabidopsis thaliana root microbiome. Since then, he has been a postdoc in the group of Detlef Weigel at the Max Planck Institute for Developmental Biology in Tübingen, Germany, studying leaf microbiomes. In the future, he is planning to focus on the interaction between plants and the bacterial genus Sphingomonas.  

22 April 2021

Experimental evidence of microbial inheritance in plants and transmission routes from seed to phyllosphere and root

Citation: Abdelfattah A, Wisniewski M, Schena L, Tack AJM.(2021). Experimental evidence of microbial inheritance in plants and transmission routes from seed to phyllosphere and root. Environmental Microbiology. doi.org/10.1111/1462-2920.15392.
 
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by Leticia Bianca Pereira

Soil is widely considered as the origin and main source of microorganisms associated with plants. However, the potential contribution of seeds to the assembly of the plant microbiome cannot be ignored. Seed microbiota remained relatively unknown, and were much less studied compared to well characterized plant compartments such as rhizosphere and phyllosphere.

Studies that demonstrate the microbiome's vertical inheritance (from seed to seedling) under natural conditions are challenging once plants are exposed to the soil with its high microbial diversity. To overcome this problem, Abdelfattah and colleagues developed a microcosm to grow common oak seedlings in microbe-free conditions while keeping the below- and aboveground plant parts separated. Using an amplicon-based approach of the ITS and 16S regions to characterize the fungal and bacterial community present in the embryo and pericarp of acorns, roots and phyllosphere of the developing seedling, the author were able to identify the transient and vertically transmitted microbiota from the seeds.

The authors found that the composition of the microbial community in embryo and pericarp greatly differed and the major part of the inherited microbiome is transmitted from the seed to the seedling. This emphasizes the ecological role of seeds as a reservoir and source for community assembly in new seedlings. Interestingly, the phyllosphere microbiota was derived mainly from the embryo microbiome, while the root microbiome represented a distinct subset of the seed microbiome. The authors also discuss the lack of information about the microbial community from embryo, since several unidentified fungal and bacterial taxa were found. Since the authors demonstrated that this seed environment is a crucial part of the vertical inheritance process, the importance of discovering of novel species that occupy this niche becomes apparent.

In summary, this study provides new information on the source and transmission of plant-associated microbes. This knowledge could increase our understanding of plant biology, and help in future biotechnological applications such as new strategies for breeding healthier crops.


About the first author : Ahmed Abdelfattah is a researcher at Institute of Environmental Biotechnology, Graz University of Technology, Austria. His research mainly focuses on microbial communities associated to plants, especially agricultural crops, including olive, citrus, strawberries, grape, wheat, and of course apples.He previously worked at Stockholm University, Sweden as postdoc to study the microbial community of oak trees with a special focus on their spatial distribution within the tree and the mechanisms of their inheritance.

14 April 2021

A complex immune response to flagellin epitope variation in commensal communities

Citation: Colaianni NR, Parys K, Lee H-S, Conway JM, Kim NH, Edelbacher N, Mucyn TS, Madalinski M, Law TF, Jones CD, et al., 2021. A complex immune response to flagellin epitope variation in commensal communities. Cell Host Microbe. doi: 10.1016/j.chom.2021.02.006.
 
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by Giannis Stringlis

In nature, plants interact with many different microbes (pathogenic, beneficial or commensal). All these microbes produce similar conserved molecules known as microbe-associated molecular patterns (MAMPs). Perception of MAMPs by specialized plant receptors, known as pattern recognition receptors or PRRs, can lead to MAMP-triggered immunity (MTI). MTI is a first layer of defense employed by plants to restrict microbial colonization and pathogenesis. One well-characterized MAMP-PRR pair is that of bacterial flagellin and FLAGELLIN SENSING 2 (FLS2). Flagellin is the building block of bacterial flagellum, required for bacterial motility, and contains flg22, a 22-amino-acid peptide known for its immune-eliciting potential. Despite the fact that different bacteria are motile due to flagellin and possess flg22 peptides, most plant niches are colonized by millions of bacteria. Therefore, a delicate interplay occurs between flg22 of plant-associated bacteria and the plant immune system.

Researchers from Dangl and Belkhadir groups aimed to characterize the flg22 repertoire of Arabidopsis commensal bacteria and their ability to induce MTI and inhibit plant growth. Genome mining in more than 600 bacterial isolates revealed their categorization in three clades, based on diversity of flagellum proteins and flg22 sequence similarity. Synthesis of 97 flg22 peptide variants (representative of the three clades) and subsequent screening for MTI, revealed that some are immunogenic (mostly from Clade I bacteria; β-/γ-Proteobacteria) while most of the peptides (mostly from Clade III bacteria; Rhizobiales, Caulobacterales) avoid to induce MTI or cause growth inhibition via different modes of action. Based on their modes of action flg22 peptides were categorized as evading (avoid MTI activation), deviant (different levels of MTI) and antagonistic (antagonizing MTI activation by immunogenic peptides). Further analysis revealed that prevalent members of rhizosphere and phyllosphere bacterial communities produce antagonistic and evading flg22 peptides, achieving as such low MTI activation and successful colonization.

Analysis of a complex synthetic microbial community colonizing roots and leaves of Arabidopsis in vitro, revealed that evading flg22 peptides are enriched in both root- and shoot-associated microbes, while the immunogenic ones are depleted. However, under conditions of salt stress, leading to a weakened plant immune system, there is enrichment of immunogenic flg22 variants in Arabidopsis-associated microbes. This finding suggests that optimal function of the immune system is required to monitor bacterial presence based on flg22 immunogenicity.

This study demonstrates that complex plant-associated bacterial communities produce a cocktail of flg22 peptides to avoid strong MTI activation and represents an important step towards understanding why some microbes are successful plant colonizers while others are not.

About the co-authors : Nicholas R. Colaianni is a PhD student in the Dangl Lab at the University of North Carolina Chapel Hill, USA.

Katarzyna Parys is a collaborator at the Gregor Mendel Institute of Molecular Plant Biology GmbH, in Vienna, Austria.

 

26 March 2021

Temperature transcends partner specificity in the symbiosis establishment of a cnidarian
Citation: Herrera M, Klein SG, Campana S, et al. Temperature transcends partner specificity in the symbiosis establishment of a cnidarian. ISME J 15, 141–153 (2021). doi.org/10.1038/s41396-020-00768-y.
 
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by Mohammad Alnajjar

Corals live in a delicate symbiotic relationship with dinoflagellate algae in the family Symbiodiniaceae. This relationship, however, is fragile and can break down in response to environmental stressors such as increased temperature, a process known as coral bleaching. As warming sea surface temperatures, consequence of climate change, become more frequent and severe, coral reef ecosystems continue to decline worldwide. Yet, contrary to increasing research efforts on coral bleaching, little is known about the establishment and development of novel symbioses in rapidly warming environments. Certainly, symbiotic flexibility is an important factor when predicting how corals might respond to increasing temperatures. Unlike other studies, Herrera et al. (From the Red Sea Research Center in KAUST/Saudi Arabia) tested different combinations of host genotypes and their native symbionts, thus taking into account genotypic variability among hosts but also the potential constraints of symbiosis and functional diversity (e.g., thermal sensitivity) within Symbiodiniaceae.

The authors used the flexible model system Exaiptasia pallida to investigate how host specificity and temperature affect the symbiosis establishment of a cnidarian. They inoculated symbiont-free anemones originating from three geographically distinct locations (Hawaii, North Carolina, and the Red Sea) using a mixture of native symbiont strains (Breviolum minutum, Symbiodinium linucheae, S. microadriaticum, and a Breviolum ecotype from the Red Sea) at ‘optimal’ and elevated temperatures and performed deep ITS2 sequencing to assess colonization dynamics across the different thermal conditions. Furthermore, they measured PSII photochemical efficiency (Fv/Fm) as a proxy of the physiological performance of symbioses over time which highlights the importance of heterotrophic feeding on the response to temperature.

This study highlights the role of temperature and partner fidelity in the establishment and performance of symbiosis and further adds to the body of work showing that pre-exposure to elevated temperature is crucial for the thermal resilience of the cnidarian holobiont. Moreover, it shows the potential of using species from the Red Sea to study thermal resilience of the cnidarian holobiont. Finally, the authors also demonstrate the importance of active feeding for enduring thermal stress.

About the first author and the group: Marcela Herrera received her PhD in Marine Science from King Abdullah University of Science and Technology (KAUST), Saudi Arabia, in June 2020. At KAUST, she worked with Professor Manuel Aranda investigating the responses of symbiotic cnidarians to environmental change. The lab focuses on understanding the mechanisms underpinning cnidarian-dinoflagellate symbiosis using a broad range of tools (genomics, bioinformatics, ecology, microbiology). Recently, Marcela started a postdoc at the Marine Eco-Evo-Devo group in the Okinawa Institute of Science and Technology (OIST), Japan, working on genomics of local adaptation of reef fish.

7 March 2021

Versatile cyanobacteria control the timing and extent of sulfide production in a Proterozoic analog microbial mat
Citation: Klatt J M, Gomez-Saez GV, Meyer S, Ristova PP, Yilmaz P, Granitsiotis MS, et al. (2020). Versatile cyanobacteria control the timing and extent of sulfide production in a Proterozoic analog microbial mat. The ISME Journal. doi:10.1038/s41396-020-0734-z.
 
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by Mohammad Alnajjar

Cyanobacterial mats were hotspots of biogeochemical cycling throughout the Proterozoic.
Contemporary cyanobacterial mats in sulfidic springs allow us to look back in time and learn about biogeochemical cycling of the past. In a contemporary cyanobacterial mat thriving in a sulfidic spring (i.e., analogue to Proterozoic) anoxygenic photosynthesis by cyanobacteria is enhancing the diel oxygen budget. This counterintuitive effect emerges because versatile cyanobacteria disrupt positive feedbacks in the classical view of the sulfur cycle. This disruption is only apparent when considering the gradual response of microbial process interactions to diel light dynamics and benthic transport phenomena. These interesting interactions were investigated by a group of scientists from Max-Planck Institute for Marine Microbiology and their colleagues from universities and research institutions in Europe and the USA, by using a broad biogeochemical and molecular toolbox. The authors found that the dissolved organic carbon (DOC) released by oxygenic photosynthesis fuels sulfide production, likely by a specialized SRB population. Increased sulfide fluxes were only stimulated after the cyanobacteria switched from anoxygenic to oxygenic photosynthesis. O2 production triggered migration of large sulfur-oxidizing bacteria from the surface to underneath the cyanobacterial layer. The resultant sulfide shield tempered anoxygenic photosynthesis and allowed the oxygenic photosynthesis to occur for a longer duration over a diel cycle. The lack of cyanobacterial DOC supply to SRB during anoxygenic photosynthesis therefore maximized O2 export. This study highlights the importance of metabolic transitions in response to dynamic environmental parameters, and of resultant interactions between processes, for ecosystem function.

About the first author: Judith Klatt is an enthusiastic young scientist, who is full of energy and bright ideas, and at the same time, a great mother. She did her PhD in the microsensor group at the Max-Planck Institute for Marine Microbiology (MPI-MM) in 2015. Then she spent 2-years as postdoc at Geomicrobiology Lab, Earth and Environmental Sciences, University of Michigan. After that, she moved back to MPI-MM to continue her journey working on sulfidic microbial mats.

7 March 2021

Diatom modulation of select bacteria through use of two unique secondary metabolites
Citation: Shibl AA, Isaac A, Ochsenkühn MA, Cárdenas A, Fei C, Behringer G, Arnoux M, Drou N, Santos MP, Gunsalus KC, Voolstra CR, Amin SA. Diatom modulation of select bacteria through use of two unique secondary metabolites. Proc Natl Acad Sci U S A. 2020 Nov 3;117(44):27445-27455.
 
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by Mohammad Alnajjar

Multicellular eukaryotes have dedicated structures to house microbiomes, whereas the mechanisms that enable diatoms and other phytoplankton species to actively modulate incoming microbes are mostly unknown. The marine microbial ecology laboratory team at the New York University in Abu-Dhabi and their colleagues from the MPI in Bremen, as well as scientists from KAUST and the University of Konstanz explored the ability of a widespread diatom, Asterionellopsis glacialis, to adopt specific mechanisms to promote association with potentially beneficial symbionts while repelling opportunists. They employed an integrated multi-omics approach (genomics, transcriptomics, metabolomics) to tease apart the functional and metabolic capacities of a bacterial consortium and a phytoplankton within a host-microbiome system. In addition, they targeted two bacterial genera, Roseobacteria and Alteromonas, to test the effects of two enigmatic secondary metabolites, azelaic acid and rosmarinic acid, on the growth and behavior of associated bacteria within the diatom photosphere. Their results suggest that a host phytoplankton cell goes through major transcriptional and metabolic reprogramming in order to modulate its microbiome through secondary metabolites. Therefore, the innate ability of an important unicellular eukaryotic group to modulate select bacteria in their microbial consortia is similar to higher eukaryotes, using unique secondary metabolites that regulate bacterial growth and behavior inversely across different bacterial populations.

About the first author: Ahmed Shibl received his PhD in Marine Science from King Abdullah University of Science and Technology (KAUST) in December 2015. At KAUST, he participated in several research expeditions to the Red Sea and Mediterranean Sea. After his doctoral studies, he spent a few months as a Postdoc in Xelu Moran’s lab (KAUST). After that, he went on a short-term visit as a Researcher in the Antunes Lab at Edge Hill University in the UK. In late 2017, he joined the Shady Amin Lab at New York University Abu Dhabi to study the diatom core microbiome and phytoplankton-bacteria interactions

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