Publications by authors named "Laura S Weyrich"

49 Publications

Effectiveness of decontamination protocols when analyzing ancient DNA preserved in dental calculus.

Sci Rep 2021 Apr 2;11(1):7456. Epub 2021 Apr 2.

Australian Centre for Ancient DNA, School of Biological Sciences, University of Adelaide, Adelaide, South Australia, Australia.

Ancient DNA analysis of human oral microbial communities within calcified dental plaque (calculus) has revealed key insights into human health, paleodemography, and cultural behaviors. However, contamination imposes a major concern for paleomicrobiological samples due to their low endogenous DNA content and exposure to environmental sources, calling into question some published results. Decontamination protocols (e.g. an ethylenediaminetetraacetic acid (EDTA) pre-digestion or ultraviolet radiation (UV) and 5% sodium hypochlorite immersion treatments) aim to minimize the exogenous content of the outer surface of ancient calculus samples prior to DNA extraction. While these protocols are widely used, no one has systematically compared them in ancient dental calculus. Here, we compare untreated dental calculus samples to samples from the same site treated with four previously published decontamination protocols: a UV only treatment; a 5% sodium hypochlorite immersion treatment; a pre-digestion in EDTA treatment; and a combined UV irradiation and 5% sodium hypochlorite immersion treatment. We examine their efficacy in ancient oral microbiota recovery by applying 16S rRNA gene amplicon and shotgun sequencing, identifying ancient oral microbiota, as well as soil and skin contaminant species. Overall, the EDTA pre-digestion and a combined UV irradiation and 5% sodium hypochlorite immersion treatment were both effective at reducing the proportion of environmental taxa and increasing oral taxa in comparison to untreated samples. This research highlights the importance of using decontamination procedures during ancient DNA analysis of dental calculus to reduce contaminant DNA.
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http://dx.doi.org/10.1038/s41598-021-86100-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8018977PMC
April 2021

Antibiotic-induced alterations and repopulation dynamics of yellowtail kingfish microbiota.

Anim Microbiome 2020 Aug 3;2(1):26. Epub 2020 Aug 3.

South Australian Research and Development Institute, Aquatic Sciences Centre, West Beach, SA, Australia.

Background: The use of antibiotics in aquaculture is a common infection treatment and is increasing in some sectors and jurisdictions. While antibiotic treatment can negatively shift gut bacterial communities, recovery and examination of these communities in fish of commercial importance is not well documented. Examining the impacts of antibiotics on farmed fish microbiota is fundamental for improving our understanding and management of healthy farmed fish. This work assessed yellowtail kingfish (Seriola lalandi) skin and gut bacterial communities after an oral antibiotic combination therapy in poor performing fish that displayed signs of enteritis over an 18-day period. In an attempt to promote improved bacterial re-establishment after antibiotic treatment, faecal microbiota transplantation (FMT) was also administered via gavage or in the surrounding seawater, and its affect was evaluated over 15 days post-delivery.

Results: Antibiotic treatment greatly perturbed the global gut bacterial communities of poor-performing fish - an effect that lasted for up to 18 days post treatment. This perturbation was marked by a significant decrease in species diversity and evenness, as well as a concomitant increase in particular taxa like an uncultured Mycoplasmataceae sp., which persisted and dominated antibiotic-treated fish for the entire 18-day period. The skin-associated bacterial communities were also perturbed by the antibiotic treatment, notably within the first 3 days; however, this was unlike the gut, as skin microbiota appeared to shift towards a more 'normal' (though disparate) state after 5 days post antibiotic treatment. FMT was only able to modulate the impacts of antibiotics in some individuals for a short time period, as the magnitude of change varied substantially between individuals. Some fish maintained certain transplanted gut taxa (i.e. present in the FMT inoculum; namely various Aliivibrio related ASVs) at Day 2 post FMT, although these were lost by Day 8 post FMT.

Conclusion: As we observed notable, prolonged perturbations induced by antibiotics on the gut bacterial assemblages, further work is required to better understand the processes/dynamics of their re-establishment following antibiotic exposure. In this regard, procedures like FMT represent a novel approach for promoting improved microbial recovery, although their efficacy and the factors that support their success requires further investigation.
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http://dx.doi.org/10.1186/s42523-020-00046-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7807502PMC
August 2020

Early markers of periodontal disease and altered oral microbiota are associated with glycemic control in children with type 1 diabetes.

Pediatr Diabetes 2021 May 15;22(3):474-481. Epub 2020 Dec 15.

Discipline of Paediatrics and Robinson Research Institute, University of Adelaide, Adelaide, South Australia, Australia.

Objectives: To determine the relationship between periodontal disease and glycemic control in children with type 1 diabetes and to characterize the diversity and composition of their oral microbiota.

Methods: Cross-sectional study including children with type 1 diabetes recruited from clinics at the Women's and Children's Hospital (Australia). Participants had a comprehensive dental assessment, periodontal examination, and buccal and gingival samples collected for 16S rRNA sequencing.

Results: Seventy-seven participants (age 13.3 ± 2.6 years, 38 males, BMI z-score 0.81 ± 0.75) had a diabetes duration of 5.6 ± 3.9 years and median HbA1c of 8.5% (range 5.8-13.3), 69.4 mmol/mol (range 39.9-121.9). Thirty-eight (49%) had early markers of periodontal disease. HbA1c was positively correlated with plaque index (Rho = 0.34, P = 0.002), gingival index (Rho = 0.30, P = 0.009), bleeding on probing (Rho = 0.44, P = 0.0001) and periodontal pocket depth >3 mm (Rho = 0.21, P = 0.06). A 1% increase in HbA1c was independently associated with an average increase in bleeding on probing of 25% (P = 0.002) and with an increase in the rate of sites with pocket depth >3 mm of 54% (P = 0.003). Higher HbA1c was independently related to increased phylogenetic alpha diversity (P = 0.008) and increased compositional variation (beta diversity P = 0.02) in gingival, but not buccal, microbiota. Brushing frequency, plaque index, and gingival index had a significant effect on microbiota composition, independent of HbA1c.

Conclusions: Children with type 1 diabetes showed a continuous relationship between less favorable glycemic control and increased early markers of periodontal disease. Glycemic control was also related to the complexity and richness of the plaque microbiota, with diversity increasing as HbA1c levels increase.
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http://dx.doi.org/10.1111/pedi.13170DOI Listing
May 2021

The evolutionary history of the human oral microbiota and its implications for modern health.

Authors:
Laura S Weyrich

Periodontol 2000 2021 Feb 23;85(1):90-100. Epub 2020 Nov 23.

Department of Anthropology and the Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, Pennsylvania, USA.

Numerous biological and cultural factors influence the microbial communities (microbiota) that inhabit the human mouth, including diet, environment, hygiene, physiology, health status, genetics, and lifestyle. As oral microbiota can underpin oral and systemic diseases, tracing the evolutionary history of oral microbiota and the factors that shape its origins will unlock information to mitigate disease today. Despite this, the origins of many oral microbes remain unknown, and the key factors in the past that shaped our oral microbiota are only now emerging. High throughput DNA sequencing of oral microbiota using ancient DNA and comparative anthropological methodologies has been employed to investigate oral microbiota origins, revealing a complex, rich history. Here, I review the current literature on the factors that shaped and guided oral microbiota evolution, both in Europe and globally. In Europe, oral microbiota evolution was shaped by interactions with Neandertals, the adaptation of farming, widespread integration of industrialization, and postindustrial lifestyles that emerged after World War II. Globally, evidence for a multitude of different oral microbiota histories is emerging, likely supporting dissimilarities in modern oral health across discrete human populations. I highlight how these evolutionary changes are linked to the development of modern oral diseases and discuss the remaining factors that need to be addressed to improve this embryonic field of research. I argue that understanding the evolutionary history of our oral microbiota is necessary to identify new treatment and prevention options to improve oral and systemic health in the future.
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http://dx.doi.org/10.1111/prd.12353DOI Listing
February 2021

The role of the oral microbiota in chronic non-communicable disease and its relevance to the Indigenous health gap in Australia.

BMC Oral Health 2020 11 16;20(1):327. Epub 2020 Nov 16.

Department of Molecular and Cellular Biology, University of Adelaide, Adelaide, SA, Australia.

Background: Aboriginal Australians and Torres Strait Islanders (hereafter respectfully referred to as Indigenous Australians) experience disproportionately poor health and low life expectancy compared to non-Indigenous Australians. Poor oral health is a critical, but understudied, contributor to this health gap. A considerable body of evidence links poor oral health to increased risks of other chronic non-communicable conditions, such as diabetes, cardiovascular disease, chronic kidney disease, and poor emotional wellbeing.  MAIN: The oral microbiota is indisputably associated with several oral diseases that disproportionately affect Indigenous Australians. Furthermore, a growing literature suggests direct and indirect links between the oral microbiota and systemic chronic non-communicable diseases that underpin much of the Indigenous health gap in Australia. Recent research indicates that oral microbial communities are shaped by a combination of cultural and lifestyle factors and are inherited from caregivers to children. Systematic differences in oral microbiota diversity and composition have been identified between Indigenous and non-Indigenous individuals in Australia and elsewhere, suggesting that microbiota-related diseases may be distinct in Indigenous Australians.  CONCLUSION: Oral microbiota research involving Indigenous Australians is a promising new area that could benefit Indigenous communities in numerous ways. These potential benefits include: (1) ensuring equity and access for Indigenous Australians in microbiota-related therapies; (2) opportunities for knowledge-sharing and collaborative research between scientists and Indigenous communities; and (3) using knowledge about the oral microbiota and chronic disease to help close the gaps in Indigenous oral and systemic health.
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http://dx.doi.org/10.1186/s12903-020-01308-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7670664PMC
November 2020

Researchers using environmental DNA must engage ethically with Indigenous communities.

Nat Ecol Evol 2021 02;5(2):146-148

School of Biological Sciences, University of Adelaide, Adelaide, South Australia, Australia.

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http://dx.doi.org/10.1038/s41559-020-01351-6DOI Listing
February 2021

Investigating the demographic history of Japan using ancient oral microbiota.

Philos Trans R Soc Lond B Biol Sci 2020 11 5;375(1812):20190578. Epub 2020 Oct 5.

Australian Centre for Ancient DNA, University of Adelaide, Adelaide, Australia.

While microbial communities in the human body (microbiota) are now commonly associated with health and disease in industrialised populations, we know very little about how these communities co-evolved and changed with humans throughout history and deep prehistory. We can now examine these communities by sequencing ancient DNA preserved within calcified dental plaque (calculus), providing insights into the origins of disease and their links to human history. Here, we examine ancient DNA preserved within dental calculus samples and their associations with two major cultural periods in Japan: the Jomon period hunter-gatherers approximately 3000 years before present (BP) and the Edo period agriculturalists 400-150 BP. We investigate how human oral microbiomes have changed in Japan through time and explore the presence of microorganisms associated with oral diseases (e.g. periodontal disease, dental caries) in ancient Japanese populations. Finally, we explore oral microbial strain diversity and its potential links to ancient demography in ancient Japan by performing phylogenomic analysis of a widely conserved oral species- oral taxon 439. This research represents, to our knowledge, the first study of ancient oral microbiomes from Japan and demonstrates that the analysis of ancient dental calculus can provide key information about the origin of non-infectious disease and its deep roots with human demography. This article is part of the theme issue 'Insights into health and disease from ancient biomolecules'.
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http://dx.doi.org/10.1098/rstb.2019.0578DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7702792PMC
November 2020

Transfer of environmental microbes to the skin and respiratory tract of humans after urban green space exposure.

Environ Int 2020 12 22;145:106084. Epub 2020 Sep 22.

Department of Molecular and Biomedical Science, University of Adelaide, Adelaide, SA 5005, Australia; Department of Anthropology, The Pennsylvania State University, University Park, PA 16802, USA; Huck Institutes of Life Sciences, The Pennsylvania State University, University Park, PA 16802, USA. Electronic address:

Background: In industrialized countries, non-communicable diseases have been increasing in prevalence since the middle of the 20th century. While the causal mechanisms remain poorly understood, increased population density, pollution, sedentary behavior, smoking, changes in diet, and limited outdoor exposure have all been proposed as significant contributors. Several hypotheses (e.g. Hygiene, Old Friends, and Biodiversity Hypotheses) also suggest that limited environmental microbial exposures may underpin part of this rise in non-communicable diseases. In response, the Microbiome Rewilding Hypothesis proposes that adequate environmental microbial exposures could be achieved by restoring urban green spaces and could potentially decrease the prevalence of non-communicable diseases. However, the microbial interactions between humans and their surrounding environment and the passaging of microbes between both entities remains poorly understood, especially within an urban context.

Results: Here, we survey human skin (n = 90 swabs) and nasal (n = 90 swabs) microbiota of three subjects that were exposed to air (n = 15), soil (n = 15), and leaves (n = 15) from different urban green space environments in three different cities across different continents (Adelaide, Australia; Bournemouth, United Kingdom; New Delhi, India). Using 16S ribosomal RNA metabarcoding, we examined baseline controls (pre-exposure) of both skin (n = 16) and nasal (n = 16) swabs and tracked microbiota transfer from the environment to the human body after exposure events. Microbial richness and phylogenetic diversity increased after urban green space exposure in skin and nasal samples collected in two of the three locations. The microbial composition of skin samples also became more similar to soil microbiota after exposure, while nasal samples became more similar to air samples. Nasal samples were more variable between sites and individuals than skin samples.

Conclusions: We show that exposure to urban green spaces can increase skin and nasal microbial diversity and alter human microbiota composition. Our study improves our understanding of human-environmental microbial interactions and suggests that increased exposure to diverse outdoor environments may increase the microbial diversity, which could lead to positive health outcomes for non-communicable diseases.
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http://dx.doi.org/10.1016/j.envint.2020.106084DOI Listing
December 2020

Investigating Both Mucosal Immunity and Microbiota in Response to Gut Enteritis in Yellowtail Kingfish.

Microorganisms 2020 Aug 20;8(9). Epub 2020 Aug 20.

School of Life and Environmental Sciences, Faculty of Sciences Engineering and Built Environment, Deakin University, Waurn Ponds, VIC 3216, Australia.

The mucosal surfaces of fish play numerous roles including, but not limited to, protection against pathogens, nutrient digestion and absorption, excretion of nitrogenous wastes and osmotic regulation. During infection or disease, these surfaces act as the first line of defense, where the mucosal immune system interacts closely with the associated microbiota to maintain homeostasis. This study evaluated microbial changes across the gut and skin mucosal surfaces in yellowtail kingfish displaying signs of gut inflammation, as well as explored the host gene expression in these tissues in order to improve our understanding of the underlying mechanisms that contribute to the emergence of these conditions. For this, we obtained and analyzed 16S rDNA and transcriptomic (RNA-Seq) sequence data from the gut and skin mucosa of fish exhibiting different health states (i.e., healthy fish and fish at the early and late stages of enteritis). Both the gut and skin microbiota were perturbed by the disease. More specifically, the gastrointestinal microbiota of diseased fish was dominated by an uncultured sp., and fish at the early stage of the disease showed a significant loss of diversity in the skin. Using transcriptomics, we found that only a few genes were significantly differentially expressed in the gut. In contrast, gene expression in the skin differed widely between health states, in particular in the fish at the late stage of the disease. These changes were associated with several metabolic pathways that were differentially expressed and reflected a weakened host. Altogether, this study highlights the sensitivity of the skin mucosal surface in response to gut inflammation.
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http://dx.doi.org/10.3390/microorganisms8091267DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7565911PMC
August 2020

Probiotic Lactobacillus Rhamnosus GG Protects Against P. Gingivalis And F. Nucleatum Gut Dysbiosis.

J Int Acad Periodontol 2020 04 1;22(2):18-27. Epub 2020 Apr 1.

Faculty of Health and Medical Sciences, Adelaide Dental School, The University of Adelaide, Adelaide, South Australia, Australia.

Objectives: This study investigated changes induced by Porphyromonas gingivalis and on gastrointestinal histology and gut microbiome in a mouse model of experimental periodontitis. The effect of probiotic Lactobacillus rhamnosus GG (LGG) in altering these changes was also investigated.

Methods: IThirty-six mice were allocated into six groups. Experimental alveolar bone loss was induced by oral inoculation with P. gingivalis and F. nucleatum. LGG was orally inoculated or orally gavaged. Gastrointestinal tissue changes were assessed using histological analysis and immunohistochemistry. Caecal microbiome was analysed by sequencing 16S rRNA genes of caecal content.

Results: Inoculation with P. gingivalis and F. nucleatum induced inflammation throughout gastrointestinal tract (p less than 0.05), increased expression of IL-6 in ileum (p = 0.052) and altered composition of caecal microbiome (p less than 0.05) in experimental mice compared to controls. Mice treated with LGG had reduced tissue inflammation in duodenum (p = 0.044) and lowered levels of IL-6 in ileum (p = 0.048) when compared with disease. LGG therapy influenced gut microbiome changes.

Conclusion: P. gingivalis and F. nucleatum inoculation induced significant changes in intestinal inflammation and caecal microbiome. Oral gavage with LGG exerted a protective effect against intestinal inflammation and limited gut microbiome changes associated with P. gingivalis and F. nucleatum.
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April 2020

Early Last Interglacial ocean warming drove substantial ice mass loss from Antarctica.

Proc Natl Acad Sci U S A 2020 02 11;117(8):3996-4006. Epub 2020 Feb 11.

South Australian Museum, Adelaide, South Australia 5005, Australia.

The future response of the Antarctic ice sheet to rising temperatures remains highly uncertain. A useful period for assessing the sensitivity of Antarctica to warming is the Last Interglacial (LIG) (129 to 116 ky), which experienced warmer polar temperatures and higher global mean sea level (GMSL) (+6 to 9 m) relative to present day. LIG sea level cannot be fully explained by Greenland Ice Sheet melt (∼2 m), ocean thermal expansion, and melting mountain glaciers (∼1 m), suggesting substantial Antarctic mass loss was initiated by warming of Southern Ocean waters, resulting from a weakening Atlantic meridional overturning circulation in response to North Atlantic surface freshening. Here, we report a blue-ice record of ice sheet and environmental change from the Weddell Sea Embayment at the periphery of the marine-based West Antarctic Ice Sheet (WAIS), which is underlain by major methane hydrate reserves. Constrained by a widespread volcanic horizon and supported by ancient microbial DNA analyses, we provide evidence for substantial mass loss across the Weddell Sea Embayment during the LIG, most likely driven by ocean warming and associated with destabilization of subglacial hydrates. Ice sheet modeling supports this interpretation and suggests that millennial-scale warming of the Southern Ocean could have triggered a multimeter rise in global sea levels. Our data indicate that Antarctica is highly vulnerable to projected increases in ocean temperatures and may drive ice-climate feedbacks that further amplify warming.
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http://dx.doi.org/10.1073/pnas.1902469117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7049167PMC
February 2020

Microbiome applications for pathology: challenges of low microbial biomass samples during diagnostic testing.

J Pathol Clin Res 2020 04 15;6(2):97-106. Epub 2020 Jan 15.

Australian Centre for Ancient DNA, Department of Molecular and Biomedical Science, University of Adelaide, Adelaide, SA, Australia.

The human microbiome can play key roles in disease, and diagnostic testing will soon have the ability to examine these roles in the context of clinical applications. Currently, most diagnostic testing in pathology applications focuses on a small number of disease-causing microbes and dismisses the whole microbial community that causes or is modulated by disease. Microbiome modifications have already provided clinically relevant insights in gut and oral diseases, such as irritable bowel disease, but there are currently limitations when clinically examining microbiomes outside of these body sites. This is critical, as the majority of microbial samples used in pathology originate from body sites that contain low concentrations of microbial DNA, including skin, tissue, blood, and urine. These samples, also known as low microbial biomass samples, are difficult to examine without careful consideration and precautions to mitigate contamination and biases. Here, we present the limitations when analysing low microbial biomass samples using current protocols and techniques and highlight the advantages that microbiome testing can offer diagnostics in the future, if the proper precautions are implemented. Specifically, we discuss the sources of contamination and biases that may result in false assessments for these sample types. Finally, we provide recommendations to mitigate contamination and biases from low microbial biomass samples during diagnostic testing, which will be especially important to effectively diagnose and treat patients using microbiome analyses.
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http://dx.doi.org/10.1002/cjp2.151DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7164373PMC
April 2020

Naturally-diverse airborne environmental microbial exposures modulate the gut microbiome and may provide anxiolytic benefits in mice.

Sci Total Environ 2020 Jan 28;701:134684. Epub 2019 Oct 28.

School of Biological Sciences and the Environment Institute, The University of Adelaide, Adelaide, South Australia 5005, Australia; College of Science and Engineering, Flinders University, Bedford Park, South Australia 5042, Australia. Electronic address:

Growing epidemiological evidence links natural green space exposure with a range of health benefits, including for mental health. Conversely, greater urbanisation associates with increased risk of mental health disorders. Microbiomes are proposed as an important but understudied link that may help explain many green space-human health associations. However, there remains a lack of controlled experimental evidence testing possible beneficial effects from passive exposure to natural biodiversity via airborne microbiota. Previous mouse model studies have used unrealistic environmental microbial exposures-including excessive soil and organic matter contact, feed supplements and injections-to demonstrate host microbiota, immune biomarker, and behavioural changes. Here, in a randomised controlled experiment, we demonstrate that realistic exposures to trace-level dust from a high biodiversity soil can change mouse gut microbiota, in comparison to dust from low biodiversity soil or no soil (control) (n = 54 total mice, comprising 3 treatments × 18 mice, with 9 females + 9 males per group). Furthermore, we found a nominal soil-derived anaerobic spore-forming butyrate-producer, Kineothrix alysoides, was supplemented to a greater extent in the gut microbiomes of high biodiversity treatment mice. Also, increasing relative abundance of this rare organism correlated with reduced anxiety-like behaviour in the most anxious mice. Our results point to an intriguing new hypothesis: that biodiverse soils may represent an important supplementary source of butyrate-producing bacteria capable of resupplying the mammalian gut microbiome, with potential for gut health and mental health benefits. Our findings have potential to inform cost-effective population health interventions through microbiome-conscious green space design and, ultimately, the mainstreaming of biodiversity into health care.
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http://dx.doi.org/10.1016/j.scitotenv.2019.134684DOI Listing
January 2020

Toolbox for the sampling and monitoring of benthic cyanobacteria.

Water Res 2020 Feb 23;169:115222. Epub 2019 Oct 23.

Water Research Centre, Department of Ecology and Evolutionary Biology, School of Biological Sciences, University of Adelaide, South Australia, 5005, Australia.

Benthic cyanobacteria are a nuisance because they produce highly potent toxins and taste and odour compounds. Despite this, benthic cyanobacteria remain far less studied than their planktonic counterparts. For example, little is known about their growth or the seasonality of their secondary metabolite production. Moreover, sampling and monitoring techniques commonly used for the survey of planktonic species are not necessarily applicable to benthic forms. This study aimed to develop and validate a new sampling device for the routine monitoring of benthic mats. Molecular monitoring techniques were established and validated on environmental samples collected in a South Australian reservoir (SA-L2). A total of eight qPCR assays were applied to samples in order to track seasonal variations in cyanobacteria concentrations and associated secondary metabolite production. Next Generation Sequencing was utilised to conduct a microbial community composition analysis and to select the most appropriate substrate material for the sampling of benthic cyanobacteria. The concentration of the secondary metabolites geosmin and 2-methyl-isoborneol were quantified using High-Performance Liquid Chromatography, and concentrations of key nutrients (N, P) were quantified in water samples. The sampling device designed proved efficient and easy to use in the field. The qPCR assay designed for the amplification of the cyanobacterial MIB synthase had a high efficiency with a minimum limit of quantification of 4 cell-equivalents per reaction and identified a potential source of MIB in SA-L2 Reservoir. The peak season for benthic growth and secondary metabolite production was observed in spring. Proportionally, 35% of the variability in water geosmin concentrations can be explained by benthic actinobacterial and cyanobacterial activity, showing that freshwater benthic mats represent a significant source of taste and odour compounds.
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http://dx.doi.org/10.1016/j.watres.2019.115222DOI Listing
February 2020

More Arrows in the Ancient DNA Quiver: Use of Paleoepigenomes and Paleomicrobiomes to Investigate Animal Adaptation to Environment.

Mol Biol Evol 2020 02;37(2):307-319

Australian Centre for Ancient DNA, School of Biological Sciences, Environment Institute, University of Adelaide, Adelaide, South Australia, Australia.

Whether and how epigenetic mechanisms and the microbiome play a role in mammalian adaptation raised considerable attention and controversy, mainly because they have the potential to add new insights into the Modern Synthesis. Recent attempts to reconcile neo-Darwinism and neo-Lamarckism in a unified theory of molecular evolution give epigenetic mechanisms and microbiome a prominent role. However, supporting empirical data are still largely missing. Because experimental studies using extant animals can hardly be done over evolutionary timescales, we propose that advances in ancient DNA techniques provide a valid alternative. In this piece, we evaluate 1) the possible roles of epigenomes and microbiomes in animal adaptation, 2) advances in the retrieval of paleoepigenome and paleomicrobiome data using ancient DNA techniques, and 3) the plasticity of either and interactions between the epigenome and the microbiome, while emphasizing that it is essential to take both into account, as well as the underlying genetic factors that may confound the findings. We propose that advanced ancient DNA techniques should be applied to a wide range of past animals, so novel dynamics in animal evolution and adaption can be revealed.
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http://dx.doi.org/10.1093/molbev/msz231DOI Listing
February 2020

City life alters the gut microbiome and stable isotope profiling of the eastern water dragon (Intellagama lesueurii).

Mol Ecol 2019 10 2;28(20):4592-4607. Epub 2019 Oct 2.

Global Change Ecology Research Group, School of Science and Engineering, University of the Sunshine Coast, Sippy Downs, Qld, Australia.

Urbanisation is one of the most significant threats to biodiversity, due to the rapid and large-scale environmental alterations it imposes on the natural landscape. It is, therefore, imperative that we understand the consequences of and mechanisms by which, species can respond to it. In recent years, research has shown that plasticity of the gut microbiome may be an important mechanism by which animals can adapt to environmental change, yet empirical evidence of this in wild non-model species remains sparse. Using an empirical replicated study system, we show that city life alters the gut microbiome and stable isotope profiling of a wild native non-model species - the eastern water dragon (Intellagama lesueurii) in Queensland, Australia. City dragons exhibit a more diverse gut microbiome than their native habitat counterparts and show gut microbial signatures of a high fat and plant rich diet. Additionally, we also show that city dragons have elevated levels of the Nitrogen-15 isotope in their blood suggesting that a city diet, which incorporates novel anthropogenic food sources, may also be richer in protein. These results highlight the role that gut microbial plasticity plays in an animals' response to human-altered landscapes.
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http://dx.doi.org/10.1111/mec.15240DOI Listing
October 2019

Minimum founding populations for the first peopling of Sahul.

Nat Ecol Evol 2019 07 17;3(7):1057-1063. Epub 2019 Jun 17.

Global Ecology, College of Science and Engineering, Flinders University, Adelaide, South Australia, Australia.

The timing, context and nature of the first people to enter Sahul is still poorly understood owing to a fragmented archaeological record. However, quantifying the plausible demographic context of this founding population is essential to determine how and why the initial peopling of Sahul occurred. We developed a stochastic, age-structured model using demographic rates from hunter-gatherer societies, and relative carrying capacity hindcasted with LOVECLIM's net primary productivity for northern Sahul. We projected these populations to determine the resilience and minimum sizes required to avoid extinction. A census founding population of between 1,300 and 1,550 individuals was necessary to maintain a quasi-extinction threshold of ≲0.1. This minimum founding population could have arrived at a single point in time, or through multiple voyages of ≥130 people over ~700-900 years. This result shows that substantial population amalgamation in Sunda and Wallacea in Marine Isotope Stages 3-4 provided the conditions for the successful, large-scale and probably planned peopling of Sahul.
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http://dx.doi.org/10.1038/s41559-019-0902-6DOI Listing
July 2019

Relating Urban Biodiversity to Human Health With the 'Holobiont' Concept.

Front Microbiol 2019 26;10:550. Epub 2019 Mar 26.

School of Biological Sciences, The Environment Institute, The University of Adelaide, Adelaide, SA, Australia.

A relatively unaccounted ecosystem service from biodiversity is the benefit to human health via symbiotic microbiota from our environment. This benefit occurs because humans evolved alongside microbes and have been constantly exposed to diverse microbiota. Plants and animals, including humans, are organised as a host with symbiotic microbiota, whose collective genome and life history form a single holobiont. As such, there are interdependencies between biodiversity, holobionts, and public health which lead us to argue that human health outcomes could be improved by increasing contact with biodiversity in an urban context. We propose that humans, like all holobionts, likely require a diverse microbial habitat to appropriate resources for living healthy, long lives. We discuss how industrial urbanisation likely disrupts the symbiosis between microbiota and their hosts, leading to negative health outcomes. The industrialised urban habitat is low in macro and microbial biodiversity and discourages contact with beneficial environmental microbiota. These habitat factors, alongside diet, antibiotics, and others, are associated with the epidemic of non-communicable diseases in these societies. We suggest that restoration of urban microbial biodiversity and micro-ecological processes through microbiome rewilding can benefit holobiont health and aid in treating the urban non-communicable disease epidemic. Further, we identify research gaps and some solutions to economic and strategic hurdles in applying microbiome rewilding into daily urban life.
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http://dx.doi.org/10.3389/fmicb.2019.00550DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6444116PMC
March 2019

Laboratory contamination over time during low-biomass sample analysis.

Mol Ecol Resour 2019 Jul 29;19(4):982-996. Epub 2019 Apr 29.

Australian Centre for Ancient DNA, University of Adelaide, Adelaide, South Australia, Australia.

Bacteria are not only ubiquitous on earth but can also be incredibly diverse within clean laboratories and reagents. The presence of both living and dead bacteria in laboratory environments and reagents is especially problematic when examining samples with low endogenous content (e.g., skin swabs, tissue biopsies, ice, water, degraded forensic samples or ancient material), where contaminants can outnumber endogenous microorganisms within samples. The contribution of contaminants within high-throughput studies remains poorly understood because of the relatively low number of contaminant surveys. Here, we examined 144 negative control samples (extraction blank and no-template amplification controls) collected in both typical molecular laboratories and an ultraclean ancient DNA laboratory over 5 years to characterize long-term contaminant diversity. We additionally compared the contaminant content within a home-made silica-based extraction method, commonly used to analyse low endogenous content samples, with a widely used commercial DNA extraction kit. The contaminant taxonomic profile of the ultraclean ancient DNA laboratory was unique compared to modern molecular biology laboratories, and changed over time according to researcher, month and season. The commercial kit also contained higher microbial diversity and several human-associated taxa in comparison to the home-made silica extraction protocol. We recommend a minimum of two strategies to reduce the impacts of laboratory contaminants within low-biomass metagenomic studies: (a) extraction blank controls should be included and sequenced with every batch of extractions and (b) the contributions of laboratory contamination should be assessed and reported in each high-throughput metagenomic study.
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http://dx.doi.org/10.1111/1755-0998.13011DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6850301PMC
July 2019

Retrospective eDNA assessment of potentially harmful algae in historical ship ballast tank and marine port sediments.

Mol Ecol 2019 05 13;28(10):2476-2485. Epub 2019 May 13.

Australian Centre for Ancient DNA, School of Biological Sciences, University of Adelaide, Adelaide, South Australia, Australia.

Microalgal bloom events can cause major ecosystem disturbances, devastate local marine economies, and endanger public health. Therefore, detecting and monitoring harmful microalgal taxa is essential to ensure effective risk management in waterways used for fisheries, aquaculture, recreational activity, and shipping. To fully understand the current status and future direction of algal bloom distributions, we need to know how populations and ecosystems have changed over time. This baseline knowledge is critical for predicting ecosystem responses to future anthropogenic change and will assist in the future management of coastal ecosystems. We explore a NGS metabarcoding approach to rapidly identify potentially harmful microalgal taxa in 63 historic and modern Australian marine port and ballast tank sediment samples. The results provide a record of past microalgal distribution and important baseline data that can be used to assess the efficacy of shipping guidelines, nutrient pollution mitigation, and predict the impact of climate change. Critically, eDNA surveys of archived sediments were able to detect harmful algal taxa that do not produce microscopic fossils, such as Chattonella, Heterosigma, Karlodinium, and Noctiluca. Our data suggest a potential increase in Australian harmful microalgal taxa over the past 30 years, and confirm ship ballast tanks as key dispersal vectors. These molecular mapping tools will assist in the creation of policies aimed at reducing the global increase and spread of harmful algal taxa and help prevent economic and public-health problems caused by harmful algal blooms.
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http://dx.doi.org/10.1111/mec.15055DOI Listing
May 2019

Contamination in Low Microbial Biomass Microbiome Studies: Issues and Recommendations.

Trends Microbiol 2019 02 26;27(2):105-117. Epub 2018 Nov 26.

Australian Centre for Ancient DNA, University of Adelaide, Adelaide, SA, Australia; Australian Research Council (ARC) Centre of Excellence for Australian Biodiversity and Heritage (CABAH), University of Adelaide, Adelaide, SA, Australia.

Next-generation sequencing approaches in microbiome research have allowed surveys of microbial communities, their genomes, and their functions with higher sensitivity than ever before. However, this sensitivity is a double-edged sword because these tools also efficiently detect contaminant DNA and cross-contamination, which can confound the interpretation of microbiome data. Therefore, there is an urgent need to integrate key controls into microbiome research to improve the integrity of microbiome studies. Here, we review how contaminant DNA and cross-contamination arise within microbiome studies and discuss their negative impacts, especially during the analysis of low microbial biomass samples. We then identify several key measures that researchers can implement to reduce the impact of contaminant DNA and cross-contamination during microbiome research. We put forward a set of minimal experimental criteria, the 'RIDE' checklist, to improve the validity of future low microbial biomass research.
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http://dx.doi.org/10.1016/j.tim.2018.11.003DOI Listing
February 2019

Consequences of colonialism: A microbial perspective to contemporary Indigenous health.

Am J Phys Anthropol 2018 10 29;167(2):423-437. Epub 2018 Aug 29.

Australian Centre for Ancient DNA, School of Biological Sciences, University of Adelaide, Adelaide, South Australia, Australia.

Nearly all Indigenous populations today suffer from worse health than their non-Indigenous counterparts, and despite interventions against known factors, this health "gap" has not improved. The human microbiome-the beneficial, diverse microbial communities that live on and within the human body-is a crucial component in developing and maintaining normal physiological health. Disrupting this ecosystem has repercussions for microbial functionality, and thus, human health. In this article, we propose that modern-day Indigenous population health may suffer from disrupted microbial ecosystems as a consequence of historical colonialism. Colonialism may have interrupted the established relationships between the environment, traditional lifeways, and microbiomes, altering the Indigenous microbiome with detrimental health consequences.
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http://dx.doi.org/10.1002/ajpa.23637DOI Listing
October 2018

Proper Authentication of Ancient DNA Is Still Essential.

Genes (Basel) 2018 Feb 26;9(3). Epub 2018 Feb 26.

Department of Genetics & Evolution, Darling Building, The University of Adelaide, North Terrace, Adelaide, SA 5005, Australia.

Santiago-Rodriguez et al. [1] report on the putative gut microbiome and resistome of Inca and Italian mummies, and find that Italian mummies exhibit higher bacterial diversity compared to the Inca mummies.[...].
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http://dx.doi.org/10.3390/genes9030122DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5867843PMC
February 2018

Coprolites reveal ecological interactions lost with the extinction of New Zealand birds.

Proc Natl Acad Sci U S A 2018 02;115(7):1546-1551

Australian Centre for Ancient DNA, University of Adelaide, Adelaide, SA 5005, Australia;

Over the past 50,000 y, biotic extinctions and declines have left a legacy of vacant niches and broken ecological interactions across global terrestrial ecosystems. Reconstructing the natural, unmodified ecosystems that preceded these events relies on high-resolution analyses of paleoecological deposits. Coprolites are a source of uniquely detailed information about trophic interactions and the behaviors, gut parasite communities, and microbiotas of prehistoric animal species. Such insights are critical for understanding the legacy effects of extinctions on ecosystems, and can help guide contemporary conservation and ecosystem restoration efforts. Here we use high-throughput sequencing (HTS) of ancient eukaryotic DNA from coprolites to reconstruct aspects of the biology and ecology of four species of extinct moa and the critically endangered kakapo parrot from New Zealand (NZ). Importantly, we provide evidence that moa and prehistoric kakapo consumed ectomycorrhizal fungi, suggesting these birds played a role in dispersing fungi that are key to NZ's natural forest ecosystems. We also provide the first DNA-based evidence that moa frequently supplemented their broad diets with ferns and mosses. Finally, we also find parasite taxa that provide insight into moa behavior, and present data supporting the hypothesis of coextinction between moa and several parasite species. Our study demonstrates that HTS sequencing of coprolites provides a powerful tool for resolving key aspects of ancient ecosystems and may rapidly provide information not obtainable by conventional paleoecological techniques, such as fossil analyses.
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http://dx.doi.org/10.1073/pnas.1712337115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5816151PMC
February 2018

The influence of Antarctic subglacial volcanism on the global iron cycle during the Last Glacial Maximum.

Nat Commun 2017 06 9;8:15425. Epub 2017 Jun 9.

Australian Centre for Ancient DNA (ACAD), The University of Adelaide, Adelaide, South Australia 5005, Australia.

Marine sediment records suggest that episodes of major atmospheric CO drawdown during the last glacial period were linked to iron (Fe) fertilization of subantarctic surface waters. The principal source of this Fe is thought to be dust transported from southern mid-latitude deserts. However, uncertainty exists over contributions to CO sequestration from complementary Fe sources, such as the Antarctic ice sheet, due to the difficulty of locating and interrogating suitable archives that have the potential to preserve such information. Here we present petrographic, geochemical and microbial DNA evidence preserved in precisely dated subglacial calcites from close to the East Antarctic Ice-Sheet margin, which together suggest that volcanically-induced drainage of Fe-rich waters during the Last Glacial Maximum could have reached the Southern Ocean. Our results support a significant contribution of Antarctic volcanism to subglacial transport and delivery of nutrients with implications on ocean productivity at peak glacial conditions.
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http://dx.doi.org/10.1038/ncomms15425DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5472753PMC
June 2017

Neanderthal behaviour, diet, and disease inferred from ancient DNA in dental calculus.

Nature 2017 04 8;544(7650):357-361. Epub 2017 Mar 8.

Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, University of Adelaide, Adelaide, South Australia, Australia.

Recent genomic data have revealed multiple interactions between Neanderthals and modern humans, but there is currently little genetic evidence regarding Neanderthal behaviour, diet, or disease. Here we describe the shotgun-sequencing of ancient DNA from five specimens of Neanderthal calcified dental plaque (calculus) and the characterization of regional differences in Neanderthal ecology. At Spy cave, Belgium, Neanderthal diet was heavily meat based and included woolly rhinoceros and wild sheep (mouflon), characteristic of a steppe environment. In contrast, no meat was detected in the diet of Neanderthals from El Sidrón cave, Spain, and dietary components of mushrooms, pine nuts, and moss reflected forest gathering. Differences in diet were also linked to an overall shift in the oral bacterial community (microbiota) and suggested that meat consumption contributed to substantial variation within Neanderthal microbiota. Evidence for self-medication was detected in an El Sidrón Neanderthal with a dental abscess and a chronic gastrointestinal pathogen (Enterocytozoon bieneusi). Metagenomic data from this individual also contained a nearly complete genome of the archaeal commensal Methanobrevibacter oralis (10.2× depth of coverage)-the oldest draft microbial genome generated to date, at around 48,000 years old. DNA preserved within dental calculus represents a notable source of information about the behaviour and health of ancient hominin specimens, as well as a unique system that is useful for the study of long-term microbial evolution.
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http://dx.doi.org/10.1038/nature21674DOI Listing
April 2017

Embracing the gut microbiota: the new frontier for inflammatory and infectious diseases.

Clin Transl Immunology 2017 Jan 20;6(1):e125. Epub 2017 Jan 20.

Malaghan Institute of Medical Research , Wellington, New Zealand.

The gut microbiota provides essential signals for the development and appropriate function of the immune system. Through this critical contribution to immune fitness, the gut microbiota has a key role in health and disease. Recent advances in the technological applications to study microbial communities and their functions have contributed to a rapid increase in host-microbiota research. Although it still remains difficult to define a so-called 'normal' or 'healthy' microbial composition, alterations in the gut microbiota have been shown to influence the susceptibility of the host to different diseases. Current translational research combined with recent technological and computational advances have enabled in-depth study of the link between microbial composition and immune function, addressing the interplay between the gut microbiota and immune responses. As such, beneficial modulation of the gut microbiota is a promising clinical target for many prevalent diseases including inflammatory bowel disease, metabolic abnormalities such as obesity, reduced insulin sensitivity and low-grade inflammation, allergy and protective immunity against infections.
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http://dx.doi.org/10.1038/cti.2016.91DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5292562PMC
January 2017

Exploring Relationships between Host Genome and Microbiome: New Insights from Genome-Wide Association Studies.

Front Microbiol 2016 12;7:1611. Epub 2016 Oct 12.

Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, The University of Adelaide, Adelaide SA, Australia.

As our understanding of the human microbiome expands, impacts on health and disease continue to be revealed. Alterations in the microbiome can result in dysbiosis, which has now been linked to subsequent autoimmune and metabolic diseases, highlighting the need to identify factors that shape the microbiome. Research has identified that the composition and functions of the human microbiome can be influenced by diet, age, sex, and environment. More recently, studies have explored how human genetic variation may also influence the microbiome. Here, we review several recent analytical advances in this new research area, including those that use genome-wide association studies to examine host genome-microbiome interactions, while controlling for the influence of other factors. We find that current research is limited by small sample sizes, lack of cohort replication, and insufficient confirmatory mechanistic studies. In addition, we discuss the importance of understanding long-term interactions between the host genome and microbiome, as well as the potential impacts of disrupting this relationship, and explore new research avenues that may provide information about the co-evolutionary history of humans and their microorganisms.
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http://dx.doi.org/10.3389/fmicb.2016.01611DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5061000PMC
October 2016

Isolating Viable Ancient Bacteria: What You Put In Is What You Get Out.

Genome Announc 2016 Aug 25;4(4). Epub 2016 Aug 25.

Australian Centre for Ancient DNA, University of Adelaide, Adelaide, Australia.

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http://dx.doi.org/10.1128/genomeA.00712-16DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5000818PMC
August 2016