Publications by authors named "Philip Hugenholtz"

339 Publications

Chemosynthetic and photosynthetic bacteria contribute differentially to primary production across a steep desert aridity gradient.

ISME J 2021 May 25. Epub 2021 May 25.

Department of Microbiology, Biomedicine Discovery Institute, Monash University, Clayton, VIC, Australia.

Desert soils harbour diverse communities of aerobic bacteria despite lacking substantial organic carbon inputs from vegetation. A major question is therefore how these communities maintain their biodiversity and biomass in these resource-limiting ecosystems. Here, we investigated desert topsoils and biological soil crusts collected along an aridity gradient traversing four climatic regions (sub-humid, semi-arid, arid, and hyper-arid). Metagenomic analysis indicated these communities vary in their capacity to use sunlight, organic compounds, and inorganic compounds as energy sources. Thermoleophilia, Actinobacteria, and Acidimicrobiia were the most abundant and prevalent bacterial classes across the aridity gradient in both topsoils and biocrusts. Contrary to the classical view that these taxa are obligate organoheterotrophs, genome-resolved analysis suggested they are metabolically flexible, with the capacity to also use atmospheric H to support aerobic respiration and often carbon fixation. In contrast, Cyanobacteria were patchily distributed and only abundant in certain biocrusts. Activity measurements profiled how aerobic H oxidation, chemosynthetic CO fixation, and photosynthesis varied with aridity. Cell-specific rates of atmospheric H consumption increased 143-fold along the aridity gradient, correlating with increased abundance of high-affinity hydrogenases. Photosynthetic and chemosynthetic primary production co-occurred throughout the gradient, with photosynthesis dominant in biocrusts and chemosynthesis dominant in arid and hyper-arid soils. Altogether, these findings suggest that the major bacterial lineages inhabiting hot deserts use different strategies for energy and carbon acquisition depending on resource availability. Moreover, they highlight the previously overlooked roles of Actinobacteriota as abundant primary producers and trace gases as critical energy sources supporting productivity and resilience of desert ecosystems.
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http://dx.doi.org/10.1038/s41396-021-01001-0DOI Listing
May 2021

Persistence and resistance: survival mechanisms of Candidatus Dormibacterota from nutrient-poor Antarctic soils.

Environ Microbiol 2021 May 24. Epub 2021 May 24.

School of Biotechnology and Biomolecular Sciences, UNSW Sydney, Randwick, NSW, 2052, Australia.

Candidatus Dormibacterota is an uncultured bacterial phylum found predominantly in soil that is present in high abundances within cold desert soils. Here, we interrogate nine metagenome-assembled genomes (MAGs), including six new MAGs derived from soil metagenomes obtained from two eastern Antarctic sites. Phylogenomic and taxonomic analyses revealed these MAGs represent four genera and five species, representing two order-level clades within Ca. Dormibacterota. Metabolic reconstructions of these MAGs revealed the potential for aerobic metabolism, and versatile adaptations enabling persistence in the 'extreme' Antarctic environment. Primary amongst these adaptations were abilities to scavenge atmospheric H and CO as energy sources, as well as using the energy derived from H oxidation to fix atmospheric CO via the Calvin-Bassham-Benson cycle, using a RuBisCO type IE. We propose that these allow Ca. Dormibacterota to persist using H oxidation and grow using atmospheric chemosynthesis in terrestrial Antarctica. Fluorescence in situ hybridization revealed Ca. Dormibacterota to be coccoid cells, 0.3-1.4 μm in diameter, with some cells exhibiting the potential for a symbiotic or syntrophic lifestyle.
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http://dx.doi.org/10.1111/1462-2920.15610DOI Listing
May 2021

Evaluation of the Microba Community Profiler for Taxonomic Profiling of Metagenomic Datasets From the Human Gut Microbiome.

Front Microbiol 2021 20;12:643682. Epub 2021 Apr 20.

Microba Life Sciences Limited, Brisbane, QLD, Australia.

A fundamental goal of microbial ecology is to accurately determine the species composition in a given microbial ecosystem. In the context of the human microbiome, this is important for establishing links between microbial species and disease states. Here we benchmark the Microba Community Profiler (MCP) against other metagenomic classifiers using 140 moderate to complex microbial communities and a standardized reference genome database. MCP generated accurate relative abundance estimates and made substantially fewer false positive predictions than other classifiers while retaining a high recall rate. We further demonstrated that the accuracy of species classification was substantially increased using the Microba Genome Database, which is more comprehensive than reference datasets used by other classifiers and illustrates the importance of including genomes of uncultured taxa in reference databases. Consequently, MCP classifies appreciably more reads than other classifiers when using their recommended reference databases. These results establish MCP as best-in-class with the ability to produce comprehensive and accurate species profiles of human gastrointestinal samples.
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http://dx.doi.org/10.3389/fmicb.2021.643682DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8093879PMC
April 2021

A rooted phylogeny resolves early bacterial evolution.

Science 2021 05;372(6542)

School of Biological Sciences, University of Bristol, Bristol BS8 1TQ, UK.

A rooted bacterial tree is necessary to understand early evolution, but the position of the root is contested. Here, we model the evolution of 11,272 gene families to identify the root, extent of horizontal gene transfer (HGT), and the nature of the last bacterial common ancestor (LBCA). Our analyses root the tree between the major clades Terrabacteria and Gracilicutes and suggest that LBCA was a free-living flagellated, rod-shaped double-membraned organism. Contrary to recent proposals, our analyses reject a basal placement of the Candidate Phyla Radiation, which instead branches sister to Chloroflexota within Terrabacteria. While most gene families (92%) have evidence of HGT, overall, two-thirds of gene transmissions have been vertical, suggesting that a rooted tree provides a meaningful frame of reference for interpreting bacterial evolution.
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http://dx.doi.org/10.1126/science.abe0511DOI Listing
May 2021

IFNλ Therapy Prevents Severe Gastrointestinal Graft-versus-Host Disease.

Blood 2021 May 5. Epub 2021 May 5.

University of Washington, United States.

Immunopathology and intestinal stem cell (ISC) loss in the gastrointestinal (GI) tract is the prima-facie manifestation of graft-versus-host disease (GVHD) and is responsible for significant mortality after allogeneic bone marrow transplantation (BMT). Approaches to prevent GVHD to date focus on immune-suppression. Here we identify interferon-lambda (IFNl, IL-28/IL-29) as a key protector of GI GVHD immunopathology, notably within the intestinal stem cell (ISC) compartment. Ifnlr1-/- mice displayed exaggerated GI GVHD and mortality independent of Paneth cells and alterations to microbiome. Ifnlr1-/- intestinal organoid growth was significantly impaired and targeted Ifnlr1 deficiency demonstrated effects intrinsic to recipient Lgr5+ ISC and NK cells. PEGylated IL-29 (PEG-rIL-29) treatment of naïve mice enhanced Lgr5+ ISC numbers and organoid growth independent of both IL-22 and type-1 IFN and modulated proliferative and apoptosis gene sets in Lgr5+ ISC. PEG-rIL-29 treatment improved survival, reduced GVHD severity, and enhanced epithelial proliferation and ISC-derived organoid growth after BMT, The preservation of ISC numbers in response to PEG-rIL-29 after BMT occurred both in the presence and absence of IFNl,-signaling in recipient NK cells. IFNl is therefore an attractive and rapidly testable approach to prevent ISC loss and immunopathology during GVHD.
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http://dx.doi.org/10.1182/blood.2020006375DOI Listing
May 2021

Metabolic flexibility allows bacterial habitat generalists to become dominant in a frequently disturbed ecosystem.

ISME J 2021 May 3. Epub 2021 May 3.

Department of Microbiology, Biomedicine Discovery Institute, Clayton, VIC, Australia.

Ecological theory suggests that habitat disturbance differentially influences distributions of habitat generalist and specialist species. While well-established for macroorganisms, this theory has rarely been explored for microorganisms. Here we tested these principles in permeable (sandy) sediments, ecosystems with much spatiotemporal variation in resource availability and physicochemical conditions. Microbial community composition and function were profiled in intertidal and subtidal sediments using 16S rRNA gene amplicon sequencing and metagenomics, yielding 135 metagenome-assembled genomes. Community composition and metabolic traits modestly varied with sediment depth and sampling date. Several taxa were highly abundant and prevalent in all samples, including within the orders Woeseiales and Flavobacteriales, and classified as habitat generalists; genome reconstructions indicate these taxa are highly metabolically flexible facultative anaerobes and adapt to resource variability by using different electron donors and acceptors. In contrast, obligately anaerobic taxa such as sulfate reducers and candidate lineage MBNT15 were less abundant overall and only thrived in more stable deeper sediments. We substantiated these findings by measuring three metabolic processes in these sediments; whereas the habitat generalist-associated processes of sulfide oxidation and fermentation occurred rapidly at all depths, the specialist-associated process of sulfate reduction was restricted to deeper sediments. A manipulative experiment also confirmed habitat generalists outcompete specialist taxa during simulated habitat disturbance. Together, these findings show metabolically flexible habitat generalists become dominant in highly dynamic environments, whereas metabolically constrained specialists are restricted to narrower niches. Thus, an ecological theory describing distribution patterns for macroorganisms likely extends to microorganisms. Such findings have broad ecological and biogeochemical ramifications.
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http://dx.doi.org/10.1038/s41396-021-00988-wDOI Listing
May 2021

Prokaryotic taxonomy and nomenclature in the age of big sequence data.

ISME J 2021 Apr 6. Epub 2021 Apr 6.

Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia.

The classification of life forms into a hierarchical system (taxonomy) and the application of names to this hierarchy (nomenclature) is at a turning point in microbiology. The unprecedented availability of genome sequences means that a taxonomy can be built upon a comprehensive evolutionary framework, a longstanding goal of taxonomists. However, there is resistance to adopting a single framework to preserve taxonomic freedom, and ever increasing numbers of genomes derived from uncultured prokaryotes threaten to overwhelm current nomenclatural practices, which are based on characterised isolates. The challenge ahead then is to reach a consensus on the taxonomic framework and to adapt and scale the existing nomenclatural code, or create a new code, to systematically incorporate uncultured taxa into the chosen framework.
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http://dx.doi.org/10.1038/s41396-021-00941-xDOI Listing
April 2021

Candidatus Eremiobacterota, a metabolically and phylogenetically diverse terrestrial phylum with acid-tolerant adaptations.

ISME J 2021 Mar 22. Epub 2021 Mar 22.

School of Biotechnology and Biomolecular Sciences, UNSW Sydney, Randwick, NSW, Australia.

Candidatus phylum Eremiobacterota (formerly WPS-2) is an as-yet-uncultured bacterial clade that takes its name from Ca. Eremiobacter, an Antarctic soil aerobe proposed to be capable of a novel form of chemolithoautotrophy termed atmospheric chemosynthesis, that uses the energy derived from atmospheric H-oxidation to fix CO through the Calvin-Benson-Bassham (CBB) cycle via type 1E RuBisCO. To elucidate the phylogenetic affiliation and metabolic capacities of Ca. Eremiobacterota, we analysed 63 public metagenome-assembled genomes (MAGs) and nine new MAGs generated from Antarctic soil metagenomes. These MAGs represent both recognized classes within Ca. Eremiobacterota, namely Ca. Eremiobacteria and UBP9. Ca. Eremiobacteria are inferred to be facultatively acidophilic with a preference for peptides and amino acids as nutrient sources. Epifluorescence microscopy revealed Ca. Eremiobacteria cells from Antarctica desert soil to be coccoid in shape. Two orders are recognized within class Ca. Eremiobacteria: Ca. Eremiobacterales and Ca. Baltobacterales. The latter are metabolically versatile, with individual members having genes required for trace gas driven autotrophy, anoxygenic photosynthesis, CO oxidation, and anaerobic respiration. UBP9, here renamed Ca. Xenobia class. nov., are inferred to be obligate heterotrophs with acidophilic adaptations, but individual members having highly divergent metabolic capacities compared to Ca. Eremiobacteria, especially with regard to respiration and central carbon metabolism. We conclude Ca. Eremiobacterota to be an ecologically versatile phylum with the potential to thrive under an array of "extreme" environmental conditions.
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http://dx.doi.org/10.1038/s41396-021-00944-8DOI Listing
March 2021

species enriched in the oral cavity of patients with RA are a source of peptidoglycan-polysaccharide polymers that can induce arthritis in mice.

Ann Rheum Dis 2021 Jan 4. Epub 2021 Jan 4.

The University of Queensland Diamantina Institute, The University of Queensland, Princess Alexandra Hospital, Woolloongabba, Queensland, Australia

Objectives: Analysis of oral dysbiosis in individuals sharing genetic and environmental risk factors with rheumatoid arthritis (RA) patients may illuminate how microbiota contribute to disease susceptibility. We studied the oral microbiota in a prospective cohort of patients with RA, first-degree relatives (FDR) and healthy controls (HC), then genomically and functionally characterised streptococcal species from each group to understand their potential contribution to RA development.

Methods: After DNA extraction from tongue swabs, targeted 16S rRNA gene sequencing and statistical analysis, we defined a microbial dysbiosis score based on an operational taxonomic unit signature of disease. After selective culture from swabs, we identified streptococci by sequencing. We examined the ability of streptococcal cell walls (SCW) from isolates to induce cytokines from splenocytes and arthritis in ZAP-70-mutant SKG mice.

Results: RA and FDR were more likely to have periodontitis symptoms. An oral microbial dysbiosis score discriminated RA and HC subjects and predicted similarity of FDR to RA. were major contributors to the score. We identified 10 out of 15 streptococcal isolates as sp. nov., a distinct sister species to . Tumour necrosis factor and interleukin 6 production in vitro differed in response to individual isolates, suggesting strain specific effects on innate immunity. Cytokine secretion was associated with the presence of proteins potentially involved in SCW synthesis. Systemic administration of SCW from RA and HC-associated strains induced similar chronic arthritis.

Conclusions: Dysbiosis-associated periodontal inflammation and barrier dysfunction may permit arthritogenic insoluble pro-inflammatory pathogen-associated molecules, like SCW, to reach synovial tissue.
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http://dx.doi.org/10.1136/annrheumdis-2020-219009DOI Listing
January 2021

Disease-associated gut microbiome and metabolome changes in patients with chronic obstructive pulmonary disease.

Nat Commun 2020 11 18;11(1):5886. Epub 2020 Nov 18.

Priority Research Centre for Healthy Lungs, Hunter Medical Research Institute, and The University of Newcastle, Newcastle, NSW, Australia.

Chronic obstructive pulmonary disease (COPD) is the third commonest cause of death globally, and manifests as a progressive inflammatory lung disease with no curative treatment. The lung microbiome contributes to COPD progression, but the function of the gut microbiome remains unclear. Here we examine the faecal microbiome and metabolome of COPD patients and healthy controls, finding 146 bacterial species differing between the two groups. Several species, including Streptococcus sp000187445, Streptococcus vestibularis and multiple members of the family Lachnospiraceae, also correlate with reduced lung function. Untargeted metabolomics identifies a COPD signature comprising 46% lipid, 20% xenobiotic and 20% amino acid related metabolites. Furthermore, we describe a disease-associated network connecting Streptococcus parasanguinis_B with COPD-associated metabolites, including N-acetylglutamate and its analogue N-carbamoylglutamate. While correlative, our results suggest that the faecal microbiome and metabolome of COPD patients are distinct from those of healthy individuals, and may thus aid in the search for biomarkers for COPD.
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http://dx.doi.org/10.1038/s41467-020-19701-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7676259PMC
November 2020

Proposal to reclassify the proteobacterial classes and , and the phylum into four phyla reflecting major functional capabilities.

Int J Syst Evol Microbiol 2020 Nov 5;70(11):5972-6016. Epub 2020 Nov 5.

Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, Australia.

The class comprises an ecologically and metabolically diverse group of bacteria best known for dissimilatory sulphate reduction and predatory behaviour. Although this lineage is the fourth described class of the phylum , it rarely affiliates with other proteobacterial classes and is frequently not recovered as a monophyletic unit in phylogenetic analyses. Indeed, one branch of the class encompassing like predators was recently reclassified into a separate proteobacterial class, the . Here we systematically explore the phylogeny of taxa currently assigned to these classes using 120 conserved single-copy marker genes as well as rRNA genes. The overwhelming majority of markers reject the inclusion of the classes and in the phylum . Instead, the great majority of currently recognized members of the class are better classified into four novel phylum-level lineages. We propose the names phyl. nov. and phyl. nov. for two of these phyla, based on the oldest validly published names in each lineage, and retain the placeholder name SAR324 for the third phylum pending formal description of type material. Members of the class represent a separate phylum for which we propose the name phyl. nov. based on priority in the literature and general recognition of the genus phyl. nov. includes the taxa previously classified in the phylum , and these reclassifications imply that the ability of sulphate reduction was vertically inherited in the rather than laterally acquired as previously inferred. Our analysis also indicates the independent acquisition of predatory behaviour in the phyla and , which is consistent with their distinct modes of action. This work represents a stable reclassification of one of the most taxonomically challenging areas of the bacterial tree and provides a robust framework for future ecological and systematic studies.
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http://dx.doi.org/10.1099/ijsem.0.004213DOI Listing
November 2020

Author Correction: A complete domain-to-species taxonomy for Bacteria and Archaea.

Nat Biotechnol 2020 Sep;38(9):1098

Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, Queensland, Australia.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41587-020-0539-7DOI Listing
September 2020

A unified catalog of 204,938 reference genomes from the human gut microbiome.

Nat Biotechnol 2021 01 20;39(1):105-114. Epub 2020 Jul 20.

European Bioinformatics Institute (EMBL-EBI), Wellcome Genome Campus, Hinxton, UK.

Comprehensive, high-quality reference genomes are required for functional characterization and taxonomic assignment of the human gut microbiota. We present the Unified Human Gastrointestinal Genome (UHGG) collection, comprising 204,938 nonredundant genomes from 4,644 gut prokaryotes. These genomes encode >170 million protein sequences, which we collated in the Unified Human Gastrointestinal Protein (UHGP) catalog. The UHGP more than doubles the number of gut proteins in comparison to those present in the Integrated Gene Catalog. More than 70% of the UHGG species lack cultured representatives, and 40% of the UHGP lack functional annotations. Intraspecies genomic variation analyses revealed a large reservoir of accessory genes and single-nucleotide variants, many of which are specific to individual human populations. The UHGG and UHGP collections will enable studies linking genotypes to phenotypes in the human gut microbiome.
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http://dx.doi.org/10.1038/s41587-020-0603-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7801254PMC
January 2021

Detection of SARS-CoV-2 RNA in commercial passenger aircraft and cruise ship wastewater: a surveillance tool for assessing the presence of COVID-19 infected travellers.

J Travel Med 2020 08;27(5)

Queensland Alliance for Environmental Health Sciences (QAEHS), The University of Queensland, 20 Cornwall Street, Woolloongabba, QLD 4103, Australia.

Background: Wastewater-based epidemiology (WBE) for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) can be an important source of information for coronavirus disease 2019 (COVID-19) management during and after the pandemic. Currently, governments and transportation industries around the world are developing strategies to minimize SARS-CoV-2 transmission associated with resuming activity. This study investigated the possible use of SARS-CoV-2 RNA wastewater surveillance from airline and cruise ship sanitation systems and its potential use as a COVID-19 public health management tool.

Methods: Aircraft and cruise ship wastewater samples (n = 21) were tested for SARS-CoV-2 using two virus concentration methods, adsorption-extraction by electronegative membrane (n = 13) and ultrafiltration by Amicon (n = 8), and five assays using reverse-transcription quantitative polymerase chain reaction (RT-qPCR) and RT-droplet digital PCR (RT-ddPCR). Representative qPCR amplicons from positive samples were sequenced to confirm assay specificity.

Results: SARS-CoV-2 RNA was detected in samples from both aircraft and cruise ship wastewater; however concentrations were near the assay limit of detection. The analysis of multiple replicate samples and use of multiple RT-qPCR and/or RT-ddPCR assays increased detection sensitivity and minimized false-negative results. Representative qPCR amplicons were confirmed for the correct PCR product by sequencing. However, differences in sensitivity were observed among molecular assays and concentration methods.

Conclusions: The study indicates that surveillance of wastewater from large transport vessels with their own sanitation systems has potential as a complementary data source to prioritize clinical testing and contact tracing among disembarking passengers. Importantly, sampling methods and molecular assays must be further optimized to maximize detection sensitivity. The potential for false negatives by both wastewater testing and clinical swab testing suggests that the two strategies could be employed together to maximize the probability of detecting SARS-CoV-2 infections amongst passengers.
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http://dx.doi.org/10.1093/jtm/taaa116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7454825PMC
August 2020

Roadmap for naming uncultivated Archaea and Bacteria.

Nat Microbiol 2020 08 8;5(8):987-994. Epub 2020 Jun 8.

National Museum of Natural Sciences, CSIC, Madrid, Spain.

The assembly of single-amplified genomes (SAGs) and metagenome-assembled genomes (MAGs) has led to a surge in genome-based discoveries of members affiliated with Archaea and Bacteria, bringing with it a need to develop guidelines for nomenclature of uncultivated microorganisms. The International Code of Nomenclature of Prokaryotes (ICNP) only recognizes cultures as 'type material', thereby preventing the naming of uncultivated organisms. In this Consensus Statement, we propose two potential paths to solve this nomenclatural conundrum. One option is the adoption of previously proposed modifications to the ICNP to recognize DNA sequences as acceptable type material; the other option creates a nomenclatural code for uncultivated Archaea and Bacteria that could eventually be merged with the ICNP in the future. Regardless of the path taken, we believe that action is needed now within the scientific community to develop consistent rules for nomenclature of uncultivated taxa in order to provide clarity and stability, and to effectively communicate microbial diversity.
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http://dx.doi.org/10.1038/s41564-020-0733-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7381421PMC
August 2020

First confirmed detection of SARS-CoV-2 in untreated wastewater in Australia: A proof of concept for the wastewater surveillance of COVID-19 in the community.

Sci Total Environ 2020 Aug 18;728:138764. Epub 2020 Apr 18.

Queensland Alliance for Environmental Health Sciences (QAEHS), The University of Queensland, 20 Cornwall Street, Woolloongabba, QLD 4103, Australia.

Infection with SARS-CoV-2, the etiologic agent of the ongoing COVID-19 pandemic, is accompanied by the shedding of the virus in stool. Therefore, the quantification of SARS-CoV-2 in wastewater affords the ability to monitor the prevalence of infections among the population via wastewater-based epidemiology (WBE). In the current work, SARS-CoV-2 RNA was concentrated from wastewater in a catchment in Australia and viral RNA copies were enumerated using reverse transcriptase quantitative polymerase chain reaction (RT-qPCR) resulting in two positive detections within a six day period from the same wastewater treatment plant (WWTP). The estimated viral RNA copy numbers observed in the wastewater were then used to estimate the number of infected individuals in the catchment via Monte Carlo simulation. Given the uncertainty and variation in the input parameters, the model estimated a median range of 171 to 1,090 infected persons in the catchment, which is in reasonable agreement with clinical observations. This work highlights the viability of WBE for monitoring infectious diseases, such as COVID-19, in communities. The work also draws attention to the need for further methodological and molecular assay validation for enveloped viruses in wastewater.
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http://dx.doi.org/10.1016/j.scitotenv.2020.138764DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7165106PMC
August 2020

Draft Genome Sequence of Limisphaera ngatamarikiensis NGM72.4, a Moderately Alkaliphilic Thermophile Belonging to the Class .

Microbiol Resour Announc 2020 Apr 30;9(18). Epub 2020 Apr 30.

School of Biological Sciences, University of Canterbury, Christchurch, New Zealand

NGM72.4 is a thermophilic representative of the class Isolated from geothermally heated subaqueous clay sediments from a Ngatamariki hotspring in Aotearoa New Zealand, the 3,908,748-bp genome was sequenced using the Illumina HiSeq 2500 platform. Annotation revealed 3,083 coding sequences, including 3,031 proteins, 3 rRNA genes, and 46 tRNA genes.
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http://dx.doi.org/10.1128/MRA.00225-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7193930PMC
April 2020

A complete domain-to-species taxonomy for Bacteria and Archaea.

Nat Biotechnol 2020 09 27;38(9):1079-1086. Epub 2020 Apr 27.

Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, Queensland, Australia.

The Genome Taxonomy Database is a phylogenetically consistent, genome-based taxonomy that provides rank-normalized classifications for ~150,000 bacterial and archaeal genomes from domain to genus. However, almost 40% of the genomes in the Genome Taxonomy Database lack a species name. We address this limitation by using commonly accepted average nucleotide identity criteria to set bounds on species and propose species clusters that encompass all publicly available bacterial and archaeal genomes. Unlike previous average nucleotide identity studies, we chose a single representative genome to serve as the effective nomenclatural 'type' defining each species. Of the 24,706 proposed species clusters, 8,792 are based on published names. We assigned placeholder names to the remaining 15,914 species clusters to provide names to the growing number of genomes from uncultivated species. This resource provides a complete domain-to-species taxonomic framework for bacterial and archaeal genomes, which will facilitate research on uncultivated species and improve communication of scientific results.
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http://dx.doi.org/10.1038/s41587-020-0501-8DOI Listing
September 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 2020 07 13;11(4):754-770. Epub 2020 Jan 13.

Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland , St Lucia, Australia.

Objective: The gut microbiome plays a key role in the development of acute graft-versus-host disease (GVHD) following allogeneic hematopoietic stem cell transplantation. Here we investigate the individual contribution of the pre- and post-transplant gut microbiome to acute GVHD using a well-studied mouse model.

Design: Wild-type mice were cohoused with IL-17RA mice, susceptible to hyperacute GVHD, either pre- or post-transplant alone or continuously (i.e., pre- and post-transplant). Fecal samples were collected from both WT and IL-17RA mice pre- and post-cohousing and post-transplant and the microbiome analyzed using metagenomic sequencing.

Results: Priming wild-type mice via cohousing pre-transplant only is insufficient to accelerate GVHD, however, accelerated disease is observed in WT mice cohoused post-transplant only. When mice are cohoused continuously, the effect of priming and exacerbation is additive, resulting in a greater acceleration of disease in WT mice beyond that seen with cohousing post-transplant only. Metagenomic analysis of the microbiome revealed pre-transplant cohousing is associated with the transfer of specific species within two as-yet-uncultured genera of the bacterial family and . Post-transplant, we observed GVHD-associated blooms of members and subsp. , and hyperacute GVHD gut microbiome distinct from that associated with delayed-onset disease (>10 days post-transplant).

Conclusion: 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.
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http://dx.doi.org/10.1080/19490976.2019.1705729DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7524395PMC
July 2020

Correction: A phylogenomic and ecological analysis of the globally abundant Marine Group II archaea (Ca. Poseidoniales ord. nov.).

ISME J 2020 Mar;14(3):878

Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St. Lucia, QLD, Australia.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41396-019-0556-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7058124PMC
March 2020

GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database.

Bioinformatics 2019 Nov 15. Epub 2019 Nov 15.

Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, Australia.

Summary: The GTDB Toolkit (GTDB-Tk) provides objective taxonomic assignments for bacterial and archaeal genomes based on the Genome Taxonomy Database (GTDB). GTDB-Tk is computationally efficient and able to classify thousands of draft genomes in parallel. Here we demonstrate the accuracy of the GTDB-Tk taxonomic assignments by evaluating its performance on a phylogenetically diverse set of 10,156 bacterial and archaeal metagenome-assembled genomes.

Availability: GTDB-Tk is implemented in Python and licensed under the GNU General Public License v3.0. Source code and documentation are available at: https://github.com/ecogenomics/gtdbtk.

Supplementary Information: Supplementary data are available at Bioinformatics online.
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http://dx.doi.org/10.1093/bioinformatics/btz848DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7703759PMC
November 2019

Faecal inoculations alter the gastrointestinal microbiome and allow dietary expansion in a wild specialist herbivore, the koala.

Anim Microbiome 2019 Aug 21;1(1). Epub 2019 Aug 21.

Hawkesbury Institute for the Environment, Western Sydney University, Sydney, New South Wales, 2753, Australia.

Background: Differences between individuals in their gastrointestinal microbiomes can lead to variation in their ability to persist on particular diets. Koalas are dietary specialists, feeding almost exclusively on Eucalyptus foliage but many individuals will not feed on particular Eucalyptus species that are adequate food for other individuals, even when facing starvation. We undertook a faecal inoculation experiment to test whether a koala's gastrointestinal (GI) microbiome influences their diet. Wild-caught koalas that initially fed on the preferred manna gum (Eucalyptus viminalis) were brought into captivity and orally inoculated with encapsulated material derived from faeces from koalas feeding on either the less preferred messmate (E. obliqua; treatment) or manna gum (control).

Results: The gastrointestinal microbiomes of wild koalas feeding primarily on manna gum were distinct from those feeding primarily on messmate. We found that the gastrointestinal microbiomes of koalas were unresponsive to dietary changes because the control koalas' GI microbiomes did not change even when the nocturnal koalas were fed exclusively on messmate overnight. We showed that faecal inoculations can assist the GI microbiomes of koalas to change as the treatment koalas' GI microbiomes became more similar to those of wild koalas feeding on messmate. There was no overall difference between the control and treatment koalas in the quantity of messmate they consumed. However, the greater the change in the koalas' GI microbiomes, the more messmate they consumed after the inoculations had established.

Conclusions: The results suggest that dietary changes can only lead to changes in the GI microbiomes of koalas if the appropriate microbial species are present, and/or that the koala gastrointestinal microbiome influences diet selection.
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http://dx.doi.org/10.1186/s42523-019-0008-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7803123PMC
August 2019

Defining the human gut host-phage network through single-cell viral tagging.

Nat Microbiol 2019 12 5;4(12):2192-2203. Epub 2019 Aug 5.

Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, Queensland, Australia.

Viral discovery is accelerating at an unprecedented rate due to continuing advances in culture-independent sequence-based analyses. One important facet of this discovery is identification of the hosts of these recently characterized uncultured viruses. To this end, we have adapted the viral tagging approach, which bypasses the need for culture-based methods to identify host-phage pairings. Fluorescently labelled anonymous virions adsorb to unlabelled anonymous bacterial host cells, which are then individually sorted as host-phage pairs, followed by genome amplification and high-throughput sequencing to establish the identities of both the host and the attached virus(es). We demonstrate single-cell viral tagging using the faecal microbiome, including cross-tagging of viruses and bacteria between human subjects. A total of 363 unique host-phage pairings were predicted, most of which were subject-specific and involved previously uncharacterized viruses despite the majority of their bacterial hosts having known taxonomy. One-fifth of these pairs were confirmed by multiple individual tagged cells. Viruses targeting more than one bacterial species were conspicuously absent in the host-phage network, suggesting that phages are not major vectors of inter-species horizontal gene transfer in the human gut. A high level of cross-reactivity between phages and bacteria from different subjects was noted despite subject-specific viral profiles, which has implications for faecal microbiota transplant therapy.
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http://dx.doi.org/10.1038/s41564-019-0526-2DOI Listing
December 2019

Evaluation of a concatenated protein phylogeny for classification of tailed double-stranded DNA viruses belonging to the order Caudovirales.

Nat Microbiol 2019 08 20;4(8):1306-1315. Epub 2019 May 20.

Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, Queensland, Australia.

Viruses of bacteria and archaea are important players in global carbon cycling as well as drivers of host evolution, yet the taxonomic classification of viruses remains a challenge due to their genetic diversity and absence of universally conserved genes. Traditional classification approaches employ a combination of phenotypic and genetic information which is no longer scalable in the era of bulk viral genome recovery through metagenomics. Here, we evaluate a phylogenetic approach for the classification of tailed double-stranded DNA viruses from the order Caudovirales by inferring a phylogeny from the concatenation of 77 single-copy protein markers using a maximum-likelihood method. Our approach is largely consistent with the International Committee on Taxonomy of Viruses, with 72 and 89% congruence at the subfamily and genus levels, respectively. Discrepancies could be attributed to misclassifications and a small number of highly mosaic genera confounding the phylogenetic signal. We also show that confidently resolved nodes in the concatenated protein tree are highly reproducible across different software and models, and conclude that the approach can serve as a framework for a rank-normalized taxonomy of most tailed double-stranded DNA viruses.
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http://dx.doi.org/10.1038/s41564-019-0448-zDOI Listing
August 2019

Functional effects of the microbiota in chronic respiratory disease.

Lancet Respir Med 2019 10 8;7(10):907-920. Epub 2019 Apr 8.

Priority Research Centre for Healthy Lungs, Hunter Medical Research Institute and The University of Newcastle, Newcastle, NSW, Australia; Centre for Inflammation, Centenary Institute, and University of Technology Sydney, NSW, Australia. Electronic address:

The composition of the lung microbiome is increasingly well characterised, with changes in microbial diversity or abundance observed in association with several chronic respiratory diseases such as asthma, cystic fibrosis, bronchiectasis, and chronic obstructive pulmonary disease. However, the precise effects of the microbiome on pulmonary health and the functional mechanisms by which it regulates host immunity are only now beginning to be elucidated. Bacteria, viruses, and fungi from both the upper and lower respiratory tract produce structural ligands and metabolites that interact with the host and alter the development and progression of chronic respiratory diseases. Here, we review recent advances in our understanding of the composition of the lung microbiome, including the virome and mycobiome, the mechanisms by which these microbes interact with host immunity, and their functional effects on the pathogenesis, exacerbations, and comorbidities of chronic respiratory diseases. We also describe the present understanding of how respiratory microbiota can influence the efficacy of common therapies for chronic respiratory disease, and the potential of manipulation of the microbiome as a therapeutic strategy. Finally, we highlight some of the limitations in the field and propose how these could be addressed in future research.
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http://dx.doi.org/10.1016/S2213-2600(18)30510-1DOI Listing
October 2019

Evolution of photosynthesis and aerobic respiration in the cyanobacteria.

Free Radic Biol Med 2019 08 29;140:200-205. Epub 2019 Mar 29.

Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, St Lucia, Queensland, Australia.

For well over a hundred years, members of the bacterial phylum Cyanobacteria have been considered strictly photosynthetic microorganisms, reflected in their classification as "blue-green algae" in the botanical code. Recently, genomes recovered from environmental sequencing surveys representing two major uncultured basal lineages (classes) of Cyanobacteria have been found to completely lack photosynthetic and CO fixation genes. The most likely explanation for this finding is that oxygenic photosynthesis was not an ancestral feature of the Cyanobacteria, and rather originated following divergence of the primary lines of descent. Here we describe recent findings on the evolution of aerobic respiration in the non-photosynthetic cyanobacterial classes, and how this has been interpreted by researchers interested in the evolution of oxygenic photosynthesis.
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http://dx.doi.org/10.1016/j.freeradbiomed.2019.03.029DOI Listing
August 2019