ISME Journal Research Articles

Interview with Professor Colin Murrell

Prof. Colin Murrell, a distinguished microbiologist and Emeritus Professor at the University of East Anglia, UK, is well known for his contributions to various areas of environmental microbiology and microbial ecology. Prof. Murrell has received several awards, including election to membership of the European Molecular Biology Organisation, the European Academy of Microbiology, the Chinese Academy of Sciences Distinguished Professor (Einstein) Award. He was awarded a highly prestigious European Research Council Advanced Grant and has been member of many editorial boards of leading microbiological journals including Environmental Microbiology and the ISME Journal. He has graduated over 60 PhD students and supervised around 150 researchers throughout his career. His research interests are immense, extending from the development of analytical tools in molecular microbial ecology to their testing in the field, which is reflected in his extensive publication list of over 350 highly cited papers in prestigious journals. His pioneering research has significantly improved our understanding of microbial processes in diverse environments, from soil to aquatic and marine ecosystems. More recently, he has extended his scientific curiosity to karst and caves, in particular to the Movile Cave in Romania, which represents a cornerstone for understanding the role of chemolithoautotrophy in caves.

Exploiting Underutilised crops

Exploiting Underutilised crops

Diversity of indigenous arbuscular mycorrhizal fungi in rhizosphere of upland rice (Oryza sativa L.) varieties in Southwest Nigeria

Diversity of indigenous arbuscular mycorrhizal fungi in rhizosphere of upland rice (Oryza sativa L.) varieties in Southwest Nigeria

Editorial: Metagenomics in Limnology and Oceanography

The publication of this special issue, “Linking metagenomics to aquatic microbial ecology,” in Limnology and Oceanography, is long overdue. But perhaps it could not have appeared in L&O any earlier. The term “metagenomics” was invented in the late 1990s to describe the retrieval of genetic information from microorganisms without preselection by PCR, which gets only the targeted gene, or by isolating and culturing the organisms in the lab, which gets only a few microbes. Before metagenomics, microbial ecologists were well on their way to identifying microorganisms by using approaches that focused on the genes for ribosomal RNA. But with few exceptions, the rRNA gene data did not say much about what the organisms do—their role in ecological and biogeochemical processes. Metagenomic data tell us about their potential roles, and the other “omic” approaches (metatranscriptomics, metaproteomics, and so on) get closer to their ongoing activity. Metagenomics and its relatives took over microbial ecology after 2000, as documented by Pep Gasol's analysis of publications in the field since 1980 (Microbial Ecology of the Oceans, third edition 2018). Pep found that metagenomics started to have an impact, as measured by citation numbers, at least 10 years ago. Until this special issue, the metagenomic wave has left L&O largely untouched. According to the Web of Science, out of the nearly 10,000 papers published in the journal since its beginning, only seven report metagenomic results. An additional two papers have metatranscriptomic data, while no L&O paper has metaproteomic or other omic data from organisms. By contrast, since its start in 2007, the ISME Journal has published 432 metagenomic papers. All seven of the L&O metagenomic papers appeared after 2009, which so happens is when I published a primer about metagenomics and other omics in the L&O Bulletin at the invitation of then editor, John Dolan. (In case you are wondering, the L&O Bulletin article is why Deputy Editor-in-Chief Maggie Xenopoulos thought of me for this piece.) My article did not exactly launch an avalanche of papers on the topic. While this special issue appears late in metagenomic history, arguably it is appearing in L&O at just about the right time. The field has evolved to the point where it can now more forcefully explore questions of interest to L&O readers, as discussed in the issue's introduction by Grossart et al. Where once even extracting DNA was challenging, metagenomic methods now can be used by many L&O readers, not just the specialists who developed the methods. These methods have also gotten cheaper. In particular, sequencing costs have declined dramatically while sequencing power has exploded beyond belief. Because of the huge decrease in costs, microbial ecologists can analyze more samples and explore ecological and biogeochemical questions that were not feasible until recently. Metagenomic-wielding investigators can now take more time points or sample more locations; replication is no longer a foreign word. In this regard, a metagenomic paper is starting to look more like a typical L&O paper. Finally, after being dominated by work in the oceans for many years, metagenomics is catching up to the range of aquatic habitats covered by L&O. Reflecting the recent growth in freshwater omics, this special issue has more freshwater papers than marine ones (16 vs. 6). I suppose purely oceanographic methods have appeared in L&O, but it seems appropriate that this freshwater-dominated special issue is coming out in a journal published by a society that started in 1936 as the Limnological Society of America. I hope this special issue will encourage more omic papers in L&O. The journal needs these papers if it is to see the latest advances in microbial ecology and microbial biogeochemistry. It would be an exaggeration to say that metagenomics needs L&O. But publication of more omic papers in L&O would signal a maturation of the field, that it is focusing less on methodology and more on understanding microbial communities and processes. Of course, metagenomics has already contributed many new insights into the ecology and biogeochemistry of microbes. This special issue shows how it can do even more.

Exploring anammox bacteria ecology to improve nitrogen removal in wastewater treatment

Exploring anammox bacteria ecology to improve nitrogen removal in wastewater treatment

Degradation of hydrogen peroxide at the ocean's surface: the influence of the microbial community on the realized thermal niche of Prochlorococcus.

Prochlorococcus, the smallest and most abundant phytoplankter in the ocean, is highly sensitive to hydrogen peroxide (HOOH), and co-occurring heterotrophs such as Alteromonas facilitate the growth of Prochlorococcus by scavenging HOOH. Temperature is also a major influence on Prochlorococcus abundance and distribution in the ocean, and studies in other photosynthetic organisms have shown that HOOH and temperature extremes can act together as synergistic stressors. To address potential synergistic effects of temperature and HOOH on Prochlorococcus growth, high- and low-temperature-adapted representative strains were cultured at ecologically relevant concentrations under a range of HOOH concentrations and temperatures. Higher concentrations of HOOH severely diminished the permissive temperature range for growth of both Prochlorococcus strains. At the permissive temperatures, the growth rates of both Prochlorococcus strains decreased as a function of HOOH, and cold temperature increased susceptibility of photosystem II to HOOH-mediated damage. Serving as a proxy for the natural community, co-cultured heterotrophic bacteria increased the Prochlorococcus growth rate under these temperatures, and expanded the permissive range of temperature for growth. These studies indicate that in the ocean, the cross-protective function of the microbial community may confer a fitness increase for Prochlorococcus at its temperature extremes, especially near the ocean surface where oxidative stress is highest. This interaction may play a substantial role in defining the realized thermal niche and habitat range of Prochlorococcus with respect to latitude.

Genomic reconstruction of multiple lineages of uncultured benthic archaea suggests distinct biogeochemical roles and ecological niches.

Abstract Correction to: The ISME Journal (2017) 11, xx–xx; doi:10.1038/ismej.2016.189 The original published author list did not list first names. The correct author names are as follows: Cassandre S Lazar, Brett J Baker, Kiley W Seitz and Andreas P Teske.

Riverbed methanotrophy sustained by high carbon conversion efficiency.

Abstract Correction to: The ISME Journal (2015) 9, 2304–2314; doi:10.1038/ismej.2015.98; published online 22 September 2015 Updated online 24 January 2017: This article was originally published under a CC BY-NC-ND 4.0 license, but has now been made available under a CC-BY 4.0 license. The PDF and HTML versions of the paper have been modified accordingly.

Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics.

Abstract Correction to: The ISME Journal (2016) 10, 400–415; doi:10.1038/ismej.2015.121; published online 21 August 2015 Updated online 21 September 2016: This article was originally published under NPG’s License to Publish, but has now been made available under a CC BY-NC-SA 4.0 license. The PDF and HTML versions of the paper have been modified accordingly.

Connectivity to the surface determines diversity patterns in subsurface aquifers of the Fennoscandian shield.

Abstract Correction to: The ISME Journal (2016) 10, XX–XX; doi:10.1038/ismej.2016.36 Updated online June 9, 2016: This article was originally published under NPG’s License to Publish, but has now been made available under a CC BY-NC-ND 4.0 license. The PDF and HTML versions have been modified accordingly.

Eat Prey, Love? Diverse Soil Cercozoa Tell Tales of Climate Change

The enormous species diversity of Cercozoa, important soil protozoans that feed on bacteria there, might provide a means for following climate change trends, according to Flemming Ekelund at the University of Copenhagen in Denmark and his collaborators. Thus, as soil dries with the changes in climate, species composition within the Cercozoa will also likely change, affecting further decomposition within this environmental niche, they say. Meanwhile, high-throughput sequencing of genomic material from soil samples can be used to follow protozoan predators and their prey. Details appeared 8 March 2016 in The ISME Journal (doi:10.1038/ismej.2016.31).

Fish gut microbiota analysis differentiates physiology and behavior of invasive Asian carp and indigenous American fish.

Abstract Correction to: The ISME Journal (2014) 8, 541–551; doi:10.1038/ismej.2013.181 Sequencing information was missing from the published article. The data can be found here: http://www.ncbi.nlm.nih.gov/sra/SRX245252 [accn. The description of the data is linked to this corrigendum as Supplementary Information.

Metagenomic and Metatranscriptomic Analysis of an Electromethanogenic Microbial Community

Researchers have described the mechanisms of extracellular electron uptake in model electrogens like Shewanella oneidensis MR-11 and Geobacter sulfurreducens2 as well as providing evidence for direct electron uptake for some methanogenic strains in BESs3. However, practical applications of BESs will require the use of mixed microbial populations to ensure performance stability by taking advantage of microbial adaptation and symbioses that can reduce the impact of environmental or operational perturbations. However, little is known about the taxonomic composition of mixed microbial biofilms that successfully drive electromethanogenesis. Even less is known about the functional association of specific genes and pathways expressed by microbial community members that enable cooperation/competition in an electromethanogenic system. Here we utilized a novel stimulus-induced metatranscriptomic approach in combination with metagenomics to identify the microbial taxa in an electromethanogenic biofilm and quantify the dynamic responses of key genes associated with electron uptake, hydrogen production/utilization and carbon dioxide fixation. Two dual-compartment bioelectrochemical systems (BES1 and BES2) were inoculated with rice paddy soil, a minimal media without additional soluble carbon sources or chemical mediators, and a 20% CO2 headspace (balance N2). The systems were operated as described in Bretschger et al.4 using a subpassage technique to accelerate the enrichment of highly active electromethanogenic communities. The stimulus-induced metatranscriptomic experiments and metagenomic analyses were executed according to methods described in Ishii et al.5 , 6. Both systems were exposed to an open circuit condition for 45 minutes and biofilms were sampled before and after the operational change (Fig. 1a, main). At the time of sampling both systems were consuming electricity and producing methane (Fig. 1a, inset). However, BES2 was consuming more electrons per unit biomass than BES2, even though both systems had roughly equivalent methane production activity. The results from the metagenomic analyses show that the same strains of methanogens, sulfate reducers and fermenters were present in BES1 and BES2; however, they were present in different relative abundances, which may explain the performance differences (Fig. 1b and c). Further, the stimuli applied to both reactors induced different functional responses from the respective communities, which also indicates that the relative abundance of species impacts how they functionally respond in BESs. Future work will address the specific interactions that correlate with these performance differences. These data yield new perspectives on the functional and taxonomic dynamics of electromethanogenic microbial communities and how they may be controlled in BESs. 1 Ross, D. E., Flynn, J. M., Baron, D. B., Gralnick, J. A. & Bond, D. R. Towards electrosynthesis in Shewanella: energetics of reversing the Mtr pathway for reductive metabolism. PloS one 6, e16649 (2011). 2 Gregory, K. B., Bond, D. R. & Lovley, D. R. Graphite electrodes as electron donors for anaerobic respiration. Environmental Microbiology 6, 596-604 (2004). 3 Lohner, S. T., Deutzmann, J. S., Logan, B. E., Leigh, J. & Spormann, A. M. Hydrogenase-independent uptake and metabolism of electrons by the archaeon Methanococcus maripaludis. The ISME journal 8, 1673-1681 (2014). 4 Bretschger, O. et al. Functional and taxonomic dynamics of an electricity-consuming methane-producing microbial community. Bioresource technology 195, 254-264 (2015). 5 Ishii, S. i. et al. A novel metatranscriptomic approach to identify gene expression dynamics during extracellular electron transfer. Nature Communications, doi:doi:10.1038/ncomms2615 (2013). 6 Ishii, S. i. et al. Microbial metabolic networks in a complex electrogenic biofilm recovered from a stimulus-induced metatranscriptomics approach. Scientific reports 5 (2015). Figure 1

16S rRNA, 18S rRNA, 70S and 80S Ribosomes: What Does the “S” Stand For?

Sequence data of small subunit rRNA (16S rRNA for prokaryotes, 18S rRNA for eukaryotes) are an integral part of every paper describing new species of microorganisms. And because of the availability of extensive ribosomal RNA sequence databases, most “cultivation-independent” studies of microbial communities in natural environments target 16S or 18S rRNA genes. I estimate that 16S or 18S rRNA genes feature in at least 70–80% of all papers in journals such as FEMS Microbiology Ecology, ISME Journal, and Microbial Ecology.

Erratum: Viruses accumulate in aging infection centers of a fungal forest pathogen

Abstract Correction to: The ISME Journal (2014) 9, 497–507; doi:10.1038/ismej.2014.145; published online 15 August 2014 Since the publication of this article, the authors have identified an error in the acknowledgements section of their paper, namely that the following decision numbers were omitted from the funding organization: Academy of Finland (decision numbers 251193 and 258520).

Erratum: Natural occurrence of microbial sulphur oxidation by long-range electron transport in the seafloor

Abstract Correction to: The ISME Journal (2014) 8, 1843–1854; doi:10.1038/ismej.2014.41; published online 27 March 2014 Since the publication of this article, the authors have identified an error within Figure 2, namely that two accession numbers for the clones in panel d (a phylogenetic tree) were incorrect.

Erratum: Microorganisms persist at record depths in the subseafloor of the Canterbury Basin

Abstract Correction to: The ISME Journal (2014) 8, 1370–1380; doi:10.1038/ismej.2013.250; published online 16 January 2014 Since the publication of this article, it has come to the authors’ attention that the study accession number deposited in the Sequence Read Archive was omitted from the article. The study accession number is ERP002102.

Erratum: The social structure of microbial community involved in colonization resistance

Abstract Correction to: The ISME Journal (2014) 8, 564–574; doi:10.1038/ismej.2013.172; published online 3 October 2013 Since the publication of this article, the authors have identified an omission in the ‘Conflict of Interest’ section. The missing statement is as follows: Dr Wenyuan Shi is a part time Chief Science Officer of C3 Jian Inc.

Erratum: Nutrients drive transcriptional changes that maintain metabolic homeostasis but alter genome architecture in Microcystis

Abstract Correction to: The ISME Journal (2014) 8, 2080–2092; doi:10.1038/ismej.2014.78; published online 23 May 2014 Since the publication of this article, the authors have noticed an incorrect axis label in one of the figures. In Figure 2b, the x axis should read ‘N-Reduced (Nitrate) Mean Normalized RPKM (log10)’.

Erratum: Phagotrophy by the picoeukaryotic green alga Micromonas: implications for Arctic Oceans

Abstract Correction to: The ISME Journal (2014) 8, 1953–1961; doi:10.1038/ismej.2014.16; published online 20 February 2014 Since the publication of this article, the authors have noticed that there is an error in the calculations of the per cell primary production rate which is presented in Figure 4, as wellas in the associated Table 1 of the article.