Publications by authors named "David L Jones"

59 Publications

High Representation of Archaea Across All Depths in Oxic and Low-pH Sediment Layers Underlying an Acidic Stream.

Front Microbiol 2020 17;11:576520. Epub 2020 Nov 17.

School of Natural Sciences, Bangor University, Bangor, United Kingdom.

Parys Mountain or Mynydd Parys (Isle of Anglesey, United Kingdom) is a mine-impacted environment, which accommodates a variety of acidophilic organisms. Our previous research of water and sediments from one of the surface acidic streams showed a high proportion of archaea in the total microbial community. To understand the spatial distribution of archaea, we sampled cores (0-20 cm) of sediment and conducted chemical analyses and taxonomic profiling of microbiomes using 16S rRNA gene amplicon sequencing in different core layers. The taxonomic affiliation of sequencing reads indicated that archaea represented between 6.2 and 54% of the microbial community at all sediment depths. Majority of archaea were associated with the order Thermoplasmatales, with the most abundant group of sequences being clustered closely with the phylotype B_DKE, followed by "E-plasma," "A-plasma," other yet uncultured Thermoplasmatales with and spp. represented in minor proportions. Thermoplasmatales were found at all depths and in the whole range of chemical conditions with their abundance correlating with sediment Fe, As, Cr, and Mn contents. The bacterial microbiome component was largely composed in all layers of sediment by members of the phyla Proteobacteria, Actinobacteria, Nitrospirae, Firmicutes, uncultured Chloroflexi (AD3 group), and Acidobacteria. This study has revealed a high abundance of Thermoplasmatales in acid mine drainage-affected sediment layers and pointed at these organisms being the main contributors to carbon, and probably to iron and sulfur cycles in this ecosystem.
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http://dx.doi.org/10.3389/fmicb.2020.576520DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7716880PMC
November 2020

Utilization of low-molecular-weight organic compounds by the filterable fraction of a lotic microbiome.

FEMS Microbiol Ecol 2021 02;97(2)

School of Natural Sciences, Bangor University, Bangor, Gwynedd, LL57 2UW, UK.

Filterable microorganisms participate in dissolved organic carbon (DOC) cycling in freshwater systems, however their exact functional role remains unknown. We determined the taxonomic identity and community dynamics of prokaryotic microbiomes in the 0.22 µm-filtered fraction and unfiltered freshwater from the Conwy River (North Wales, UK) in microcosms and, using targeted metabolomics and 14C-labelling, examined their role in the utilization of amino acids, organic acids and sugars spiked at environmentally-relevant (nanomolar) concentrations. To identify changes in community structure, we used 16S rRNA amplicon and shotgun sequencing. Unlike the unfiltered water samples where the consumption of DOC was rapid, the filtered fraction showed a 3-day lag phase before the consumption started. Analysis of functional categories of clusters of orthologous groups of proteins (COGs) showed that COGs associated with energy production increased in number in both fractions with substrate addition. The filtered fraction utilized low-molecular-weight (LMW) DOC at much slower rates than the whole community. Addition of nanomolar concentrations of LMW DOC did not measurably influence the composition of the microbial community nor the rate of consumption across all substrate types in either fraction. We conclude that due to their low activity, filterable microorganisms play a minor role in LMW DOC processing within a short residence time of lotic freshwater systems.
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http://dx.doi.org/10.1093/femsec/fiaa244DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7864478PMC
February 2021

Spatial co-localisation of extreme weather events: a clear and present danger.

Ecol Lett 2021 Jan 12;24(1):60-72. Epub 2020 Oct 12.

School of Natural Sciences, Bangor University, Bangor, Gwynedd, LL57 2UW, UK.

Extreme weather events have become a dominant feature of the narrative surrounding changes in global climate with large impacts on ecosystem stability, functioning and resilience; however, understanding of their risk of co-occurrence at the regional scale is lacking. Based on the UK Met Office's long-term temperature and rainfall records, we present the first evidence demonstrating significant increases in the magnitude, direction of change and spatial co-localisation of extreme weather events since 1961. Combining this new understanding with land-use data sets allowed us to assess the likely consequences on future agricultural production and conservation priority areas. All land-uses are impacted by the increasing risk of at least one extreme event and conservation areas were identified as the hotspots of risk for the co-occurrence of multiple event types. Our findings provide a basis to regionally guide land-use optimisation, land management practices and regulatory actions preserving ecosystem services against multiple climate threats.
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http://dx.doi.org/10.1111/ele.13620DOI Listing
January 2021

Shedding of SARS-CoV-2 in feces and urine and its potential role in person-to-person transmission and the environment-based spread of COVID-19.

Sci Total Environ 2020 Dec 31;749:141364. Epub 2020 Jul 31.

Centre for Environmental Biotechnology, School of Natural Sciences, Bangor University, Bangor, Gwynedd LL57 2UW, UK; School of Ocean Sciences, Bangor University, Menai Bridge, Anglesey LL59 5AB, UK.

The recent detection of SARS-CoV-2 RNA in feces has led to speculation that it can be transmitted via the fecal-oral/ocular route. This review aims to critically evaluate the incidence of gastrointestinal (GI) symptoms, the quantity and infectivity of SARS-CoV-2 in feces and urine, and whether these pose an infection risk in sanitary settings, sewage networks, wastewater treatment plants, and the wider environment (e.g. rivers, lakes and marine waters). A review of 48 independent studies revealed that severe GI dysfunction is only evident in a small number of COVID-19 cases, with 11 ± 2% exhibiting diarrhea and 12 ± 3% exhibiting vomiting and nausea. In addition to these cases, SARS-CoV-2 RNA can be detected in feces from some asymptomatic, mildly- and pre-symptomatic individuals. Fecal shedding of the virus peaks in the symptomatic period and can persist for several weeks, but with declining abundances in the post-symptomatic phase. SARS-CoV-2 RNA is occasionally detected in urine, but reports in fecal samples are more frequent. The abundance of the virus genetic material in both urine (ca. 10-10 gc/ml) and feces (ca. 10-10 gc/ml) is much lower than in nasopharyngeal fluids (ca. 10-10 gc/ml). There is strong evidence of multiplication of SARS-CoV-2 in the gut and infectious virus has occasionally been recovered from both urine and stool samples. The level and infectious capability of SARS-CoV-2 in vomit remain unknown. In comparison to enteric viruses transmitted via the fecal-oral route (e.g. norovirus, adenovirus), the likelihood of SARS-CoV-2 being transmitted via feces or urine appears much lower due to the lower relative amounts of virus present in feces/urine. The biggest risk of transmission will occur in clinical and care home settings where secondary handling of people and urine/fecal matter occurs. In addition, while SARS-CoV-2 RNA genetic material can be detected by in wastewater, this signal is greatly reduced by conventional treatment. Our analysis also suggests the likelihood of infection due to contact with sewage-contaminated water (e.g. swimming, surfing, angling) or food (e.g. salads, shellfish) is extremely low or negligible based on very low predicted abundances and limited environmental survival of SARS-CoV-2. These conclusions are corroborated by the fact that tens of million cases of COVID-19 have occurred globally, but exposure to feces or wastewater has never been implicated as a transmission vector.
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http://dx.doi.org/10.1016/j.scitotenv.2020.141364DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7836549PMC
December 2020

Wastewater and public health: the potential of wastewater surveillance for monitoring COVID-19.

Curr Opin Environ Sci Health 2020 Oct 12;17:14-20. Epub 2020 Jun 12.

School of Natural Sciences, Bangor University, Deiniol Road, Bangor, Gwynedd, UK.

Pathogenic viruses represent one of the greatest threats to human well-being. As evidenced by the COVID-19 global pandemic, however, halting the spread of highly contagious diseases is notoriously difficult. Successful control strategies therefore have to rely on effective surveillance. Here, we describe how monitoring wastewater from urban areas can be used to detect the arrival and subsequent decline of pathogens, such as SARS-CoV-2. As the amount of virus shed in faeces and urine varies largely from person to person, it is very difficult to quantitatively determine the number of people who are infected in the population. More research on the surveillance of viruses in wastewater using accurate and validated methods, as well as subsequent risk analysis and modelling is paramount in understanding the dynamics of viral outbreaks.
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http://dx.doi.org/10.1016/j.coesh.2020.06.001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7291992PMC
October 2020

Negative influence of biofilm on CoCrMo corrosion.

J Biomed Mater Res A 2019 11 8;107(11):2556-2566. Epub 2019 Aug 8.

Stryker, Mahwah, New Jersey.

Minimal studies exist investigating biofilm-induced corrosion of orthopaedic implants. This study investigates potential contributions of Pseudomonas aeruginosa and Staphylococcus aureus biofilms on corrosion resistance of CoCrMo under static and fretting conditions. Biofilms were cultured on CoCrMo coupons for either 4 weeks (static culture) or 6 days (fretting culture; pin-on-disk with a Ti6Al4V hemispherical tip pin). Morphology of biofilms and corrosion of coupon surfaces were analyzed via SEM. Open circuit potential and electrochemical impedance spectroscopy measurements were collected for corrosion performance evaluation. Results showed no visible corrosion on coupon surfaces in static culture, which suggests these biofilms alone do not induce severe corrosion under the conditions of this study. However, electrochemical data showed biofilm presence lowered coupon electrochemical impedance in static and fretting cultures, suggesting resistive and capacitive characteristics of the metal oxide-biofilm-media interface were altered. Under fretting, the P. aeruginosa group exhibited a distinct damage morphology and Co:Cr:Mo ratio within the wear scar when compared with S. aureus and the bacteria-free control. These differences suggest the presence of P. aeruginosa biofilms may negatively impact corrosion resistance at the fretting interface. Taken together these results demonstrate biofilms can contribute to implant corrosion by influencing the electrochemical impedance of implant metal surfaces.
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http://dx.doi.org/10.1002/jbm.a.36761DOI Listing
November 2019

Correction to: Long-Term Recovery of Microbial Communities in the Boreal Bryosphere Following Fire Disturbance.

Microb Ecol 2020 Feb;79(2):516

School of Environment and Forest Science, University of Washington, Seattle, WA, 98195, USA.

The original version of this article contained an error in the Molecular Analysis subsection of the Methods.
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http://dx.doi.org/10.1007/s00248-019-01408-5DOI Listing
February 2020

Opinions of Speech-Language Pathologists Regarding Speech Management for Children With Cleft Lip and Palate.

Cleft Palate Craniofac J 2020 01 20;57(1):55-64. Epub 2019 Jun 20.

Division of Communication Disorders, University of Wyoming, Laramie, WY, USA.

Objective: The purpose of the present study was to examine practice patterns and opinions that speech-language pathologists (SLPs) have about speech-language intervention for children with cleft lip and palate.

Methods: One hundred seven speech-language pathology members of the American Speech-Language-Hearing Association Special Interest Group 5: Craniofacial and Velopharyngeal Disorders Special Interest Group completed a 37-item online survey that examined common practices in early intervention as well as opinions about speech characteristics, assessment, and management strategies for children with cleft lip and palate.

Results: The overwhelming majority of respondents (96%) agreed that speech-language pathologists (SLPs) should meet with parents before palatal surgery to discuss speech-language issues. Although 90% of the SLPs identified increasing consonant inventory as an early intervention goal, lack of consensus was evident regarding the type of consonant to stimulate. Respondents agreed that while blowing activities are not useful in strengthening labial, lingual, or velopharyngeal movements, they are useful in heightening awareness of oral airflow for children with cleft palate. A large degree of variability was evident in opinions regarding prevalence and treatment of compensatory articulations as well as the effectiveness of treatment strategies designed to reduce perceived hypernasality and audible nasal emission.

Conclusions: The findings of this study indicate a large degree of variability in opinions of SLP respondents regarding assessment and treatment of children with cleft lip and palate.
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http://dx.doi.org/10.1177/1055665619857000DOI Listing
January 2020

Archaea dominate the microbial community in an ecosystem with low-to-moderate temperature and extreme acidity.

Microbiome 2019 01 28;7(1):11. Epub 2019 Jan 28.

School of Natural Sciences, Bangor University, Deiniol Rd, Bangor, LL57 2UW, UK.

Background: The current view suggests that in low-temperature acidic environments, archaea are significantly less abundant than bacteria. Thus, this study of the microbiome of Parys Mountain (Anglesey, UK) sheds light on the generality of this current assumption. Parys Mountain is a historically important copper mine and its acid mine drainage (AMD) water streams are characterised by constant moderate temperatures (8-18 °C), extremely low pH (1.7) and high concentrations of soluble iron and other metal cations.

Results: Metagenomic and SSU rRNA amplicon sequencing of DNA from Parys Mountain revealed a significant proportion of archaea affiliated with Euryarchaeota, which accounted for ca. 67% of the community. Within this phylum, potentially new clades of Thermoplasmata were overrepresented (58%), with the most predominant group being "E-plasma", alongside low-abundant Cuniculiplasmataceae, 'Ca. Micrarchaeota' and 'Terrestrial Miscellaneous Euryarchaeal Group' (TMEG) archaea, which were phylogenetically close to Methanomassilicoccales and clustered with counterparts from acidic/moderately acidic settings. In the sediment, archaea and Thermoplasmata contributed the highest numbers in V3-V4 amplicon reads, in contrast with the water body community, where Proteobacteria, Nitrospirae, Acidobacteria and Actinobacteria outnumbered archaea. Cultivation efforts revealed the abundance of archaeal sequences closely related to Cuniculiplasma divulgatum in an enrichment culture established from the filterable fraction of the water sample. Enrichment cultures with unfiltered samples showed the presence of Ferrimicrobium acidiphilum, C. divulgatum, 'Ca. Mancarchaeum acidiphilum Mia14', 'Ca. Micrarchaeota'-related and diverse minor (< 2%) bacterial metagenomic reads.

Conclusion: Contrary to expectation, our study showed a high abundance of archaea in this extremely acidic mine-impacted environment. Further, archaeal populations were dominated by one particular group, suggesting that they are functionally important. The prevalence of archaea over bacteria in these microbiomes and their spatial distribution patterns represents a novel and important advance in our understanding of acidophile ecology. We also demonstrated a procedure for the specific enrichment of cell wall-deficient members of the archaeal component of this community, although the large fraction of archaeal taxa remained unculturable. Lastly, we identified a separate clustering of globally occurring acidophilic members of TMEG that collectively belong to a distinct order within Thermoplasmata with yet unclear functional roles in the ecosystem.
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http://dx.doi.org/10.1186/s40168-019-0623-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6350386PMC
January 2019

Nano-Sized and Filterable Bacteria and Archaea: Biodiversity and Function.

Front Microbiol 2018 21;9:1971. Epub 2018 Aug 21.

School of Biological Sciences, Bangor University, Bangor, United Kingdom.

Nano-sized and filterable microorganisms are thought to represent the smallest living organisms on earth and are characterized by their small size (50-400 nm) and their ability to physically pass through <0.45 μm pore size filters. They appear to be ubiquitous in the biosphere and are present at high abundance across a diverse range of habitats including oceans, rivers, soils, and subterranean bedrock. Small-sized organisms are detected by culture-independent and culture-dependent approaches, with most remaining uncultured and uncharacterized at both metabolic and taxonomic levels. Consequently, their significance in ecological roles remain largely unknown. Successful isolation, however, has been achieved for some species (e.g., and " Pelagibacter ubique"). In many instances, small-sized organisms exhibit a significant genome reduction and loss of essential metabolic pathways required for a free-living lifestyle, making their survival reliant on other microbial community members. In these cases, the nano-sized prokaryotes can only be co-cultured with their 'hosts.' This paper analyses the recent data on small-sized microorganisms in the context of their taxonomic diversity and potential functions in the environment.
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http://dx.doi.org/10.3389/fmicb.2018.01971DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6110929PMC
August 2018

Safety and immunogenicity of Pfs25H-EPA/Alhydrogel, a transmission-blocking vaccine against Plasmodium falciparum: a randomised, double-blind, comparator-controlled, dose-escalation study in healthy Malian adults.

Lancet Infect Dis 2018 09 27;18(9):969-982. Epub 2018 Jul 27.

Laboratory of Malaria Immunology and Vaccinology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, USA. Electronic address:

Background: Pfs25H-EPA is a protein-protein conjugate transmission-blocking vaccine against Plasmodium falciparum that is safe and induces functional antibodies in malaria-naive individuals. In this field trial, we assessed Pfs25H-EPA/Alhydrogel for safety and functional immunogenicity in Malian adults.

Methods: This double-blind, randomised, comparator-controlled, dose-escalation trial in Bancoumana, Mali, was done in two staggered phases, an initial pilot safety assessment and a subsequent main phase. Healthy village residents aged 18-45 years were eligible if they had normal laboratory results (including HIV, hepatitis B, hepatitis C tests) and had not received a previous malaria vaccine or recent immunosuppressive drugs, vaccines, or blood products. Participants in the pilot safety cohort and the main cohort were assigned (1:1) by block randomisation to a study vaccine group. Participants in the pilot safety cohort received two doses of Pfs25H-EPA/Alhydrogel 16 μg or Euvax B (comparator vaccine), and participants in the main cohort received Pfs25H-EPA/Alhydrogel 47 μg or comparator vaccine (Euvax B for the first, second, and third vaccinations and Menactra for the fourth vaccination). Participants and investigators were masked to group assignment, and randomisation codes in sealed envelopes held by a site pharmacist. Vials with study drug for injection were covered by opaque tape and labelled with a study identification number. Group assignments were unmasked at final study visit. The primary outcomes were safety and tolerability for all vaccinees. The secondary outcome measure was immunogenicity 14 days after vaccination in the per-protocol population, as confirmed by the presence of antibodies against Pfs25H measured by ELISA IgG and antibody functionality assessed by standard membrane feeding assays and by direct skin feeding assays. This trial is registered with ClinicalTrials.gov, number NCT01867463.

Findings: Between May 15, and Jun 16, 2013, 230 individuals were screened for eligibility. 20 individuals were enrolled in the pilot safety cohort; ten participants were assigned to receive Pfs25H-EPA/Alhydrogel 16 μg, and ten participants were assigned to receive comparator vaccine. 100 individuals were enrolled in the main cohort; 50 participants were assigned to receive Pfs25H-EPA/Alhydrogel 47 μg, and 50 participants were assigned to receive comparator vaccine. Compared with comparator vaccinees, Pfs25H vaccinees had more solicited adverse events (137 events vs 86 events; p=0·022) and treatment-related adverse events (191 events vs 126 events, p=0·034), but the number of other adverse events did not differ between study vaccine groups (792 vs 683). Pfs25H antibody titres increased with each dose, with a peak geometric mean of 422·3 ELISA units (95% CI 290-615) after the fourth dose, but decreased relatively rapidly thereafter, with a half-life of 42 days for anti-Pfs25H and 59 days for anti-EPA (median ratio of titres at day 600 to peak, 0·19 for anti-Pfs25H vs 0·29 for anti-EPA; p=0·009). Serum transmission-reducing activity was greater for Pfs25H than for comparator vaccine after the fourth vaccine dose (p<0·001) but not after the third dose (p=0·09). Repeated direct skin feeds were well tolerated, but the number of participants who infected at least one mosquito did not differ between Pfs25H and comparator vaccinees after the fourth dose (p=1, conditional exact).

Interpretation: Pfs25H-EPA/Alhydrogel was well tolerated and induced significant serum activity by standard membrane feeding assays but transmission blocking activity was not confirmed by weekly direct skin feed. This activity required four doses, and titres decreased rapidly after the fourth dose. Alternative antigens or combinations should be assessed to improve activity.

Funding: Division of Intramural Research, National Institute of Allergy and Infectious Diseases.
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http://dx.doi.org/10.1016/S1473-3099(18)30344-XDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6287938PMC
September 2018

Viromic Analysis of Wastewater Input to a River Catchment Reveals a Diverse Assemblage of RNA Viruses.

mSystems 2018 May-Jun;3(3). Epub 2018 May 22.

Microbiology Research Group, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

Detection of viruses in the environment is heavily dependent on PCR-based approaches that require reference sequences for primer design. While this strategy can accurately detect known viruses, it will not find novel genotypes or emerging and invasive viral species. In this study, we investigated the use of viromics, i.e., high-throughput sequencing of the biosphere's viral fraction, to detect human-/animal-pathogenic RNA viruses in the Conwy river catchment area in Wales, United Kingdom. Using a combination of filtering and nuclease treatment, we extracted the viral fraction from wastewater and estuarine river water and sediment, followed by high-throughput RNA sequencing (RNA-Seq) analysis on the Illumina HiSeq platform, for the discovery of RNA virus genomes. We found a higher richness of RNA viruses in wastewater samples than in river water and sediment, and we assembled a complete norovirus genotype GI.2 genome from wastewater effluent, which was not contemporaneously detected by conventional reverse transcription-quantitative PCR (qRT-PCR). The simultaneous presence of diverse rotavirus signatures in wastewater indicated the potential for zoonotic infections in the area and suggested runoff from pig farms as a possible origin of these viruses. Our results show that viromics can be an important tool in the discovery of pathogenic viruses in the environment and can be used to inform and optimize reference-based detection methods provided appropriate and rigorous controls are included. Enteric viruses cause gastrointestinal illness and are commonly transmitted through the fecal-oral route. When wastewater is released into river systems, these viruses can contaminate the environment. Our results show that we can use viromics to find the range of potentially pathogenic viruses that are present in the environment and identify prevalent genotypes. The ultimate goal is to trace the fate of these pathogenic viruses from origin to the point where they are a threat to human health, informing reference-based detection methods and water quality management.
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http://dx.doi.org/10.1128/mSystems.00025-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5964442PMC
May 2018

Detecting macroecological patterns in bacterial communities across independent studies of global soils.

Nat Microbiol 2018 02 20;3(2):189-196. Epub 2017 Nov 20.

Natural England, Exeter, UK.

The emergence of high-throughput DNA sequencing methods provides unprecedented opportunities to further unravel bacterial biodiversity and its worldwide role from human health to ecosystem functioning. However, despite the abundance of sequencing studies, combining data from multiple individual studies to address macroecological questions of bacterial diversity remains methodically challenging and plagued with biases. Here, using a machine-learning approach that accounts for differences among studies and complex interactions among taxa, we merge 30 independent bacterial data sets comprising 1,998 soil samples from 21 countries. Whereas previous meta-analysis efforts have focused on bacterial diversity measures or abundances of major taxa, we show that disparate amplicon sequence data can be combined at the taxonomy-based level to assess bacterial community structure. We find that rarer taxa are more important for structuring soil communities than abundant taxa, and that these rarer taxa are better predictors of community structure than environmental factors, which are often confounded across studies. We conclude that combining data from independent studies can be used to explore bacterial community dynamics, identify potential 'indicator' taxa with an important role in structuring communities, and propose hypotheses on the factors that shape bacterial biogeography that have been overlooked in the past.
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http://dx.doi.org/10.1038/s41564-017-0062-xDOI Listing
February 2018

Resemblance profiles as clustering decision criteria: Estimating statistical power, error, and correspondence for a hypothesis test for multivariate structure.

Ecol Evol 2017 Apr 26;7(7):2039-2057. Epub 2017 Feb 26.

College of Marine Science University of South Florida Saint Petersburg FL USA.

Clustering data continues to be a highly active area of data analysis, and resemblance profiles are being incorporated into ecological methodologies as a hypothesis testing-based approach to clustering multivariate data. However, these new clustering techniques have not been rigorously tested to determine the performance variability based on the algorithm's assumptions or any underlying data structures. Here, we use simulation studies to estimate the statistical error rates for the hypothesis test for multivariate structure based on dissimilarity profiles (DISPROF). We concurrently tested a widely used algorithm that employs the unweighted pair group method with arithmetic mean (UPGMA) to estimate the proficiency of clustering with DISPROF as a decision criterion. We simulated unstructured multivariate data from different probability distributions with increasing numbers of objects and descriptors, and grouped data with increasing overlap, overdispersion for ecological data, and correlation among descriptors within groups. Using simulated data, we measured the resolution and correspondence of clustering solutions achieved by DISPROF with UPGMA against the reference grouping partitions used to simulate the structured test datasets. Our results highlight the dynamic interactions between dataset dimensionality, group overlap, and the properties of the descriptors within a group (i.e., overdispersion or correlation structure) that are relevant to resemblance profiles as a clustering criterion for multivariate data. These methods are particularly useful for multivariate ecological datasets that benefit from distance-based statistical analyses. We propose guidelines for using DISPROF as a clustering decision tool that will help future users avoid potential pitfalls during the application of methods and the interpretation of results.
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http://dx.doi.org/10.1002/ece3.2760DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5383504PMC
April 2017

Associations between metal exposure and lesion formation in offshore Gulf of Mexico fishes collected after the Deepwater Horizon oil spill.

Mar Pollut Bull 2017 Apr 14;117(1-2):462-477. Epub 2017 Feb 14.

College of Marine Science, University of South Florida, 140 7th Ave. South, St. Petersburg, FL 33701, USA.

The objectives of this study were to: (1) examine patterns of short- and long-term metal exposure within the otoliths of six offshore fish species in varying states of health, as indicated by the presence of external skin lesions, and (2) determine if there was a change in otolith metal concentrations concurrent with the Deepwater Horizon (DWH) oil spill. Otoliths collected from 2011 to 2013 in the Gulf of Mexico (GOM) were analyzed for a suite of trace metals known to be associated with DWH oil. We found that lesioned fish often had elevated levels of otolith Ni and Zn before, during, and after the DWH oil spill. In addition, metal exposure varied according to species-specific life history patterns. These findings indicate that lesioned individuals were exposed to a persistent source of trace-metals in the GoM prior to the oil spill.
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http://dx.doi.org/10.1016/j.marpolbul.2017.01.066DOI Listing
April 2017

Critical Review on the Public Health Impact of Norovirus Contamination in Shellfish and the Environment: A UK Perspective.

Food Environ Virol 2017 06 7;9(2):123-141. Epub 2017 Feb 7.

Centre for Applied Marine Sciences, School of Ocean Sciences, Bangor University, Menai Bridge, Anglesey, LL59 5AB, UK.

We review the risk of norovirus (NoV) infection to the human population from consumption of contaminated shellfish. From a UK perspective, risk is apportioned for different vectors of NoV infection within the population. NoV spreads mainly by person-to-person contact or via unsanitary food handling. NoV also enters the coastal zone via wastewater discharges resulting in contamination of shellfish waters. Typically, NoV persists in the marine environment for several days, with its presence strongly linked to human population density, wastewater discharge rate, and efficacy of wastewater treatment. Shellfish bioaccumulate NoV and current post-harvest depuration is inefficient in its removal. While NoV can be inactivated by cooking (e.g. mussels), consumption of contaminated raw shellfish (e.g. oysters) represents a risk to human health. Consumption of contaminated food accounts for 3-11% of NoV cases in the UK (~74,000 cases/year), of which 16% are attributable to oyster consumption (11,800 cases/year). However, environmental and human factors influencing NoV infectivity remain poorly understood. Lack of standard methods for accurate quantification of infective and non-infective (damaged) NoV particles represent a major barrier, hampering identification of an appropriate lower NoV contamination limit for shellfish. Future management strategies may include shellfish quality assessment (at point of harvest or at point of supply) or harvesting controls. However, poor understanding of NoV inactivation in shellfish and the environment currently limits accurate apportionment and risk assessment for NoV and hence the identification of appropriate shellfish or environmental quality standards.
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http://dx.doi.org/10.1007/s12560-017-9279-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5429388PMC
June 2017

Long-Term Recovery of Microbial Communities in the Boreal Bryosphere Following Fire Disturbance.

Microb Ecol 2017 01 18;73(1):75-90. Epub 2016 Aug 18.

School of Environment and Forest Science, University of Washington, Seattle, WA, 98195, USA.

Our study used a ∼360-year fire chronosequence in northern Sweden to investigate post-fire microbial community dynamics in the boreal bryosphere (the living and dead parts of the feather moss layer on the forest floor, along with the associated biota). We anticipated systematic changes in microbial community structure and growth strategy with increasing time since fire (TSF) and used amplicon pyrosequencing to establish microbial community structure. We also recorded edaphic factors (relating to pH, C and N accumulation) and the physical characteristics of the feather moss layer. The molecular analyses revealed an unexpectedly diverse microbial community. The structure of the community could be largely explained by just two factors, TSF and pH, although the importance of TSF diminished as the forest recovered from disturbance. The microbial communities on the youngest site (TSF = 14 years) were clearly different from older locations (>100 years), suggesting relatively rapid post-fire recovery. A shift towards Proteobacterial taxa on older sites, coupled with a decline in the relative abundance of Acidobacteria, suggested an increase in resource availability with TSF. Saprotrophs dominated the fungal community. Mycorrhizal fungi appeared to decline in abundance with TSF, possibly due to changing N status. Our study provided evidence for the decadal-scale legacy of burning, with implications for boreal forests that are expected to experience more frequent burns over the course of the next century.
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http://dx.doi.org/10.1007/s00248-016-0832-7DOI Listing
January 2017

Development and Clinical Evaluation of an mHealth Application for Stress Management.

Front Psychiatry 2016 26;7:130. Epub 2016 Jul 26.

Philadelphia VA Medical Center, University of Pennsylvania , Philadelphia, PA , USA.

A large number of individuals experience mental health disorders, with cognitive behavioral therapy (CBT) emerging as a standard practice for reduction in psychiatric symptoms, including stress, anger, anxiety, and depression. However, CBT is associated with significant patient dropout and lacks the means to provide objective data regarding a patient's experience and symptoms between sessions. Emerging wearables and mobile health (mHealth) applications represent an approach that may provide objective data to the patient and provider between CBT sessions. Here, we describe the development of a classifier of real-time physiological stress in a healthy population (n = 35) and apply it in a controlled clinical evaluation for armed forces veterans undergoing CBT for stress and anger management (n = 16). Using cardiovascular and electrodermal inputs from a wearable device, the classifier was able to detect physiological stress in a non-clinical sample with accuracy greater than 90%. In a small clinical sample, patients who used the classifier and an associated mHealth application were less likely to discontinue therapy (p = 0.016, d = 1.34) and significantly improved on measures of stress (p = 0.032, d = 1.61), anxiety (p = 0.050, d = 1.26), and anger (p = 0.046, d = 1.41) compared to controls undergoing CBT alone. Given the large number of individuals that experience mental health disorders and the unmet need for treatment, especially in developing nations, such mHealth approaches have the potential to provide or augment treatment at low cost in the absence of in-person care.
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http://dx.doi.org/10.3389/fpsyt.2016.00130DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4960497PMC
August 2016

Spatial patterns and environmental constraints on ecosystem services at a catchment scale.

Sci Total Environ 2016 Dec 5;572:1586-1600. Epub 2016 May 5.

School of Environment, Natural Resources and Geography, Bangor University, Bangor, Gwynedd LL57 2UW, UK.

Improved understanding and prediction of the fundamental environmental controls on ecosystem service supply across the landscape will help to inform decisions made by policy makers and land-water managers. To evaluate this issue for a local catchment case study, we explored metrics and spatial patterns of service supply for water quality regulation, agriculture production, carbon storage, and biodiversity for the Macronutrient Conwy catchment. Methods included using ecosystem models such as LUCI and JULES, integration of national scale field survey datasets, earth observation products and plant trait databases, to produce finely resolved maps of species richness and primary production. Analyses were done with both 1×1km gridded and subcatchment data. A common single gradient characterised catchment scale ecosystem services supply with agricultural production and carbon storage at opposing ends of the gradient as reported for a national-scale assessment. Species diversity was positively related to production due to the below national average productivity levels in the Conwy combined with the unimodal relationship between biodiversity and productivity at the national scale. In contrast to the national scale assessment, a strong reduction in water quality as production increased was observed in these low productive systems. Various soil variables were tested for their predictive power of ecosystem service supply. Soil carbon, nitrogen, their ratio and soil pH all had double the power of rainfall and altitude, each explaining around 45% of variation but soil pH is proposed as a potential metric for ecosystem service supply potential as it is a simple and practical metric which can be carried out in the field with crowd-sourcing technologies now available. The study emphasises the importance of considering multiple ecosystem services together due to the complexity of covariation at local and national scales, and the benefits of exploiting a wide range of metrics for each service to enhance data robustness.
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http://dx.doi.org/10.1016/j.scitotenv.2016.04.004DOI Listing
December 2016

Strategic assessment of fisheries independent monitoring programs in the gulf of Mexico.

PLoS One 2015 2;10(3):e0120929. Epub 2015 Apr 2.

University of South Florida-College of Marine Science, 140 7th Ave S, St. Petersburg, Florida, 33701, United States of America.

This study evaluates information produced from 14 fisheries independent monitoring programs (FIM) in the Gulf of Mexico. We consider the uniqueness of information from each program and its usefulness in estimating fisheries management indices. Biomass values of 35 functional groups are extracted from an operating model (Ecospace) with a method that replicates the patterns of historic FIM samplings. Observation error is added to these data in order to create a set of pseudo data that replicate the type and quality of information obtained from FIM programs. The pseudo data were put into a separate fishery assessment model (Pella-Tomlinson) to determine management indices of each functional group (maximum sustainable yield (MSY), biomass at MSY, and fishing mortality at MSY). These indices are compared against values in Ecospace, and against previously published single-species stock assessments. We also evaluate the full suite of information derived from FIM within an ecosystem context, considering whether functional roles are over- or under-sampled, and whether sampling effort is proportional to the value of fish stocks. Results reveal that model derived fishery indices closely matched published indices for the majority of the functional groups, economic and ecological evaluation suggests that several piscivorous functional groups are under-sampled include forage base species that are likely to indirectly support fisheries for piscivores, and sampling efforts are not proportional to the value of some fish stocks. Following ecological modelling we performed statistical analyses on historic FIM catch data to identify optimal species-specific sampling months and gear-types that can be used to refine future FIM sampling efforts.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0120929PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4383601PMC
March 2016

Spatial and temporal heterogeneity of bacteria across an intertidal shellfish bed: implications for regulatory monitoring of faecal indicator organisms.

Sci Total Environ 2015 Feb 14;506-507:1-9. Epub 2014 Nov 14.

Centre for Applied Marine Sciences, Bangor University, Menai Bridge, Anglesey LL59 5AB, UK. Electronic address:

Routine bacterial monitoring of shellfish beds using indicator species is a common global practice designed to prevent human consumption of contaminated shellfish products. However, current bacteriological monitoring procedures which focus on the quantification of faecal indicator organisms (FIOs) as a proxy for microbial pollution may not be representative of total bacterial contamination levels present in shellfish harvesting areas. The objective of this study was to critically assess the accuracy of current monitoring strategies by quantifying the spatial (lateral and longitudinal distance) and temporal (seasonality and tidal state) concentrations of FIOs (Escherichia coli and total coliforms) within a single intertidal commercially harvested shellfish bed. Spatial and temporal FIO dynamics, including the effects of tidal state and seasonality, were quantified in mussel flesh and sediment samples from a single intertidal mussel (Mytilus edulis) bed. Our results confirmed that FIO concentrations across a shellfish bed were heterogeneous over larger spatial and temporal scales, but showed no relation to the concentrations of autochthonous bacteria, such as Vibrio spp., or the physico-chemical parameters of the sediment. These results have important implications for both public health and the economic prosperity of the shellfish industry, and demonstrate the importance of accommodating both spatial and temporal fluctuations in routine bacteriological monitoring protocols. We conclude that current FIO monitoring procedures may not accurately represent levels of microbial contamination within shellfish harvesting areas and that more robust microbiological testing procedures need developing.
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http://dx.doi.org/10.1016/j.scitotenv.2014.10.100DOI Listing
February 2015

Distribution and diversity of members of the bacterial phylum Fibrobacteres in environments where cellulose degradation occurs.

Syst Appl Microbiol 2014 Oct 17;37(7):502-9. Epub 2014 Jul 17.

School of Biological Sciences and Natural Resources and Geography, Bangor University, Deiniol Road, Bangor, Gwynedd LL57 2UW, UK. Electronic address:

The Fibrobacteres phylum contains two described species, Fibrobacter succinogenes and Fibrobacter intestinalis, both of which are prolific degraders of cellulosic plant biomass in the herbivore gut. However, recent 16S rRNA gene sequencing studies have identified novel Fibrobacteres in landfill sites, freshwater lakes and the termite hindgut, suggesting that members of the Fibrobacteres occupy a broader ecological range than previously appreciated. In this study, the ecology and diversity of Fibrobacteres was evaluated in 64 samples from contrasting environments where cellulose degradation occurred. Fibrobacters were detected in 23 of the 64 samples using Fibrobacter genus-specific 16S rRNA gene PCR, which provided their first targeted detection in marine and estuarine sediments, cryoconite from Arctic glaciers, as well as a broader range of environmental samples. To determine the phylogenetic diversity of the Fibrobacteres phylum, Fibrobacter-specific 16S rRNA gene clone libraries derived from 17 samples were sequenced (384 clones) and compared with all available Fibrobacteres sequences in the Ribosomal Database Project repository. Phylogenetic analysis revealed 63 lineages of Fibrobacteres (95% OTUs), with many representing as yet unclassified species. Of these, 24 OTUs were exclusively comprised of fibrobacters derived from environmental (non-gut) samples, 17 were exclusive to the mammalian gut, 15 to the termite hindgut, and 7 comprised both environmental and mammalian strains, thus establishing Fibrobacter spp. as indigenous members of microbial communities beyond the gut ecosystem. The data highlighted significant taxonomic and ecological diversity within the Fibrobacteres, a phylum circumscribed by potent cellulolytic activity, suggesting considerable functional importance in the conversion of lignocellulosic biomass in the biosphere.
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http://dx.doi.org/10.1016/j.syapm.2014.06.001DOI Listing
October 2014

Evaluation of dissolved organic carbon as a soil quality indicator in national monitoring schemes.

PLoS One 2014 14;9(3):e90882. Epub 2014 Mar 14.

Centre for Ecology and Hydrology, Environment Centre Wales, Bangor, Gwynedd, United Kingdom.

Background: Monitoring the properties of dissolved organic carbon (DOC) in soil water is frequently used to evaluate changes in soil quality and to explain shifts in freshwater ecosystem functioning.

Methods: Using >700 individual soils (0-15 cm) collected from a 209,331 km(2) area we evaluated the relationship between soil classification (7 major soil types) or vegetation cover (8 dominant classes, e.g. cropland, grassland, forest) and the absorbance properties (254 and 400 nm), DOC quantity and quality (SUVA, total soluble phenolics) of soil water.

Results: Overall, a good correlation (r(2)= 0.58) was apparent between soil water absorbance and DOC concentration across the diverse range of soil types tested. In contrast, both DOC and the absorbance properties of soil water provided a poor predictor of SUVA or soluble phenolics which we used as a measure of humic substance concentration. Significant overlap in the measured ranges for UV absorbance, DOC, phenolic content and especially SUVA of soil water were apparent between the 8 vegetation and 7 soil classes. A number of significant differences, however, were apparent within these populations with total soluble phenolics giving the greatest statistical separation between both soil and vegetation groups.

Conclusions: We conclude that the quality of DOC rather than its quantity provides a more useful measure of soil quality in large scale surveys.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0090882PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3954595PMC
December 2014

Auxin secretion by Bacillus amyloliquefaciens FZB42 both stimulates root exudation and limits phosphorus uptake in Triticum aestivium.

BMC Plant Biol 2014 Feb 21;14:51. Epub 2014 Feb 21.

School of Environment, Natural Resources and Geography, College of Natural Sciences, Bangor University, Bangor, Gwynedd LL57 2DG, UK.

Background: The use of auxin-producing rhizosphere bacteria as agricultural products promises increased root production and therefore greater phosphate (Pi) uptake. Whilst such bacteria promote root production in vitro, the nature of the bacteria-plant interaction in live soil, particularly concerning any effects on nutrient uptake, are not known. This study uses Bacillus amyloliquefaciens FZB42, an auxin-producing rhizobacterium, as a dressing on Triticum aestivium seeds. It then examines the effects on root production, Pi uptake, Pi-related gene expression and organic carbon (C) exudation.

Results: Seed treatment with B. amyloliquefaciens FZB42 increased root production at low environmental Pi concentrations, but significantly repressed root Pi uptake. This coincided with an auxin-mediated reduction in expression of the Pi transporters TaPHT1.8 and TaPHT1.10. Applied exogenous auxin also triggered an increase in root C exudation. At high external Pi concentrations, root production was promoted by B. amyloliquefaciens FZB42, but Pi uptake was unaffected.

Conclusions: We conclude that, alongside promoting root production, auxin biosynthesis by B. amyloliquefaciens FZB42 both re-models Pi transporter expression and elevates organic C exudation. This shows the potential importance of rhizobacterial-derived auxin following colonisation of root surfaces, and the nature of this bacteria-plant interaction in soil.
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http://dx.doi.org/10.1186/1471-2229-14-51DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4015440PMC
February 2014

Competition between plant and bacterial cells at the microscale regulates the dynamics of nitrogen acquisition in wheat (Triticum aestivum).

New Phytol 2013 Nov 12;200(3):796-807. Epub 2013 Jul 12.

Soil Biology and Molecular Ecology Group, School of Earth and Environment, Institute of Agriculture, University of Western Australia, Crawley, WA, 6009, Australia.

The ability of plants to compete effectively for nitrogen (N) resources is critical to plant survival. However, controversy surrounds the importance of organic and inorganic sources of N in plant nutrition because of our poor ability to visualize and understand processes happening at the root-microbial-soil interface. Using high-resolution nano-scale secondary ion mass spectrometry stable isotope imaging (NanoSIMS-SII), we quantified the fate of ¹⁵N over both space and time within the rhizosphere. We pulse-labelled the soil surrounding wheat (Triticum aestivum) roots with either ¹⁵NH₄⁺ or ¹⁵N-glutamate and traced the movement of ¹⁵N over 24 h. Imaging revealed that glutamate was rapidly depleted from the rhizosphere and that most ¹⁵N was captured by rhizobacteria, leading to very high ¹⁵N microbial enrichment. After microbial capture, approximately half of the ¹⁵N-glutamate was rapidly mineralized, leading to the excretion of NH₄⁺, which became available for plant capture. Roots proved to be poor competitors for ¹⁵N-glutamate and took up N mainly as ¹⁵NH₄⁺. Spatial mapping of ¹⁵N revealed differential patterns of ¹⁵N uptake within bacteria and the rapid uptake and redistribution of ¹⁵N within roots. In conclusion, we demonstrate the rapid cycling and transformation of N at the soil-root interface and that wheat capture of organic N is low in comparison to inorganic N under the conditions tested.
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http://dx.doi.org/10.1111/nph.12405DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3916831PMC
November 2013

A systematic review of the effectiveness of liming to mitigate impacts of river acidification on fish and macro-invertebrates.

Environ Pollut 2013 Aug 22;179:285-93. Epub 2013 May 22.

School of Environment, Natural Resources & Geography, Bangor University, Deiniol Road, Bangor LL57 2UW, UK.

The addition of calcium carbonate to catchments or watercourses--liming--has been used widely to mitigate freshwater acidification but the abatement of acidifying emissions has led to questions about its effectiveness and necessity. We conducted a systematic review and meta-analysis of the impact of liming streams and rivers on two key groups of river organisms: fish and invertebrates. On average, liming increased the abundance and richness of acid-sensitive invertebrates and increased overall fish abundance, but benefits were variable and not guaranteed in all rivers. Where B-A-C-I designs (before-after-control-impact) were used to reduce bias, there was evidence that liming decreased overall invertebrate abundance. This systematic review indicates that liming has the potential to mitigate the symptoms of acidification in some instances, but effects are mixed. Future studies should use robust designs to isolate recovery due to liming from decreasing acid deposition, and assess factors affecting liming outcomes.
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http://dx.doi.org/10.1016/j.envpol.2013.04.019DOI Listing
August 2013

Bioreduction of sheep carcasses effectively contains and reduces pathogen levels under operational and simulated breakdown conditions.

Environ Sci Technol 2013 May 2;47(10):5267-75. Epub 2013 May 2.

School of Environment, Natural Resources & Geography, College of Natural Sciences, Bangor University, Gwynedd, LL57 2UW, UK.

Options for the storage and disposal of animal carcasses are extremely limited in the EU after the introduction of the EU Animal By-products Regulations (ABPR; EC/1774/2002), leading to animosity within the livestock sector and the call for alternative methods to be validated. Novel storage technologies such as bioreduction may be approved under the ABPR provided that they can be shown to prevent pathogen proliferation. We studied the survival of Enterococcus faecalis, Salmonella spp., E. coli O157 and porcine parvovirus in bioreduction vessels containing sheep carcasses for approximately 4 months. The vessels were operated under two different scenarios: (A) where the water within was aerated and heated to 40 °C, and (B) with no aeration or heating, to simulate vessel failure. Microbial analysis verified that pathogens were contained within the bioreduction vessel and indeed reduced in numbers with time under both scenarios. This study shows that bioreduction can provide an effective and safe on-farm storage system for livestock carcasses prior to ultimate disposal. The findings support a review of the current regulatory framework so that bioreduction is considered for approval for industry use within the EU.
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http://dx.doi.org/10.1021/es400183zDOI Listing
May 2013

The Fibrobacteres: an important phylum of cellulose-degrading bacteria.

Microb Ecol 2012 Feb 3;63(2):267-81. Epub 2012 Jan 3.

School of Biological Sciences, Bangor University, Bangor, Gwynedd, LL57 2UW, UK.

The phylum Fibrobacteres currently comprises one formal genus, Fibrobacter, and two cultured species, Fibrobacter succinogenes and Fibrobacter intestinalis, that are recognised as major bacterial degraders of lignocellulosic material in the herbivore gut. Historically, members of the genus Fibrobacter were thought to only occupy mammalian intestinal tracts. However, recent 16S rRNA gene-targeted molecular approaches have demonstrated that novel centres of variation within the genus Fibrobacter are present in landfill sites and freshwater lakes, and their relative abundance suggests a potential role for fibrobacters in cellulose degradation beyond the herbivore gut. Furthermore, a novel subphylum within the Fibrobacteres has been detected in the gut of wood-feeding termites, and proteomic analyses have confirmed their involvement in cellulose hydrolysis. The genome sequence of F. succinogenes rumen strain S85 has recently suggested that within this group of organisms a "third" way of attacking the most abundant form of organic carbon in the biosphere, cellulose, has evolved. This observation not only has evolutionary significance, but the superior efficiency of anaerobic cellulose hydrolysis by Fibrobacter spp., in comparison to other cellulolytic rumen bacteria that typically utilise membrane-bound enzyme complexes (cellulosomes), may be explained by this novel cellulase system. There are few bacterial phyla with potential functional importance for which there is such a paucity of phenotypic and functional data. In this review, we highlight current knowledge of the Fibrobacteres phylum, its taxonomy, phylogeny, ecology and potential as a source of novel glycosyl hydrolases of biotechnological importance.
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http://dx.doi.org/10.1007/s00248-011-9998-1DOI Listing
February 2012

Fate of pathogens in a simulated bioreduction system for livestock carcasses.

Waste Manag 2012 May 26;32(5):933-8. Epub 2011 Nov 26.

School of Environment, Natural Resources & Geography, College of Natural Sciences, Bangor University, Gwynedd LL57 2UW, UK.

The EU Animal By-Products Regulations generated the need for novel methods of storage and disposal of dead livestock. Bioreduction prior to rendering or incineration has been proposed as a practical and potentially cost-effective method; however, its biosecurity characteristics need to be elucidated. To address this, Salmonella enterica (serovars Senftenberg and Poona), Enterococcus faecalis, Campylobacter jejuni, Campylobacter coli and a lux-marked strain of Escherichia coli O157 were inoculated into laboratory-scale bioreduction vessels containing sheep carcass constituents. Numbers of all pathogens and the metabolic activity of E. coli O157 decreased significantly within the liquor waste over time, and only E. faecalis remained detectable after 3months. Only very low numbers of Salmonella spp. and E. faecalis were detected in bioaerosols, and only at initial stages of the trial. These results further indicate that bioreduction represents a suitable method of storing and reducing the volume of livestock carcasses prior to ultimate disposal.
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http://dx.doi.org/10.1016/j.wasman.2011.10.031DOI Listing
May 2012