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1. Functional diversity of microbial ecologies estimated from ancient human coprolites and dental calculus

   https://doi.org/10.1098/rstb.2019.0586  

   Jacobson, David K.; Honap, Tanvi P.; Monroe, Cara; Lund, Justin; Houk, Brett A.; Novotny, Anna C.; Robin, Cynthia; Marini, Elisabetta; Lewis, Cecil M. (November 2020, Philosophical Transactions of the Royal Society B: Biological Sciences)

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   Human microbiome studies are increasingly incorporating macroecological approaches, such as community assembly, network analysis and functional redundancy to more fully characterize the microbiome. Such analyses have not been applied to ancient human microbiomes, preventing insights into human microbiome evolution. We address this issue by analysing published ancient microbiome datasets: coprolites from Rio Zape ( n = 7; 700 CE Mexico) and historic dental calculus ( n = 44; 1770–1855 CE, UK), as well as two novel dental calculus datasets: Maya ( n = 7; 170 BCE-885 CE, Belize) and Nuragic Sardinians ( n = 11; 1400–850 BCE, Italy). Periodontitis-associated bacteria ( Treponema denticola , Fusobacterium nucleatum and Eubacterium saphenum ) were identified as keystone taxa in the dental calculus datasets. Coprolite keystone taxa included known short-chain fatty acid producers ( Eubacterium biforme, Phascolarctobacterium succinatutens ) and potentially disease-associated bacteria ( Escherichia , Brachyspira) . Overlap in ecological profiles between ancient and modern microbiomes was indicated by similarity in functional response diversity profiles between contemporary hunter–gatherers and ancient coprolites, as well as parallels between ancient Maya, historic UK, and modern Spanish dental calculus; however, the ancient Nuragic dental calculus shows a distinct ecological structure. We detected key ecological signatures from ancient microbiome data, paving the way to expand understanding of human microbiome evolution. This article is part of the theme issue ‘Insights into health and disease from ancient biomolecules’. 

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2. Identification of the Bacterial Biosynthetic Gene Clusters of the Oral Microbiome Illuminates the Unexplored Social Language of Bacteria during Health and Disease

   https://doi.org/10.1128/mBio.00321-19  

   Aleti, Gajender; Baker, Jonathon L.; Tang, Xiaoyu; Alvarez, Ruth; Dinis, Márcia; Tran, Nini C.; Melnik, Alexey V.; Zhong, Cuncong; Ernst, Madeleine; Dorrestein, Pieter C.; et al (April 2019, mBio)

   ABSTRACT Small molecules are the primary communication media of the microbial world. Recent bioinformatic studies, exploring the biosynthetic gene clusters (BGCs) which produce many small molecules, have highlighted the incredible biochemical potential of the signaling molecules encoded by the human microbiome. Thus far, most research efforts have focused on understanding the social language of the gut microbiome, leaving crucial signaling molecules produced by oral bacteria and their connection to health versus disease in need of investigation. In this study, a total of 4,915 BGCs were identified across 461 genomes representing a broad taxonomic diversity of oral bacteria. Sequence similarity networking provided a putative product class for more than 100 unclassified novel BGCs. The newly identified BGCs were cross-referenced against 254 metagenomes and metatranscriptomes derived from individuals either with good oral health or with dental caries or periodontitis. This analysis revealed 2,473 BGCs, which were differentially represented across the oral microbiomes associated with health versus disease. Coabundance network analysis identified numerous inverse correlations between BGCs and specific oral taxa. These correlations were present in healthy individuals but greatly reduced in individuals with dental caries, which may suggest a defect in colonization resistance. Finally, corroborating mass spectrometry identified several compounds with homology to products of the predicted BGC classes. Together, these findings greatly expand the number of known biosynthetic pathways present in the oral microbiome and provide an atlas for experimental characterization of these abundant, yet poorly understood, molecules and socio-chemical relationships, which impact the development of caries and periodontitis, two of the world’s most common chronic diseases. IMPORTANCE The healthy oral microbiome is symbiotic with the human host, importantly providing colonization resistance against potential pathogens. Dental caries and periodontitis are two of the world’s most common and costly chronic infectious diseases and are caused by a localized dysbiosis of the oral microbiome. Bacterially produced small molecules, often encoded by BGCs, are the primary communication media of bacterial communities and play a crucial, yet largely unknown, role in the transition from health to dysbiosis. This study provides a comprehensive mapping of the BGC repertoire of the human oral microbiome and identifies major differences in health compared to disease. Furthermore, BGC representation and expression is linked to the abundance of particular oral bacterial taxa in health versus dental caries and periodontitis. Overall, this study provides a significant insight into the chemical communication network of the healthy oral microbiome and how it devolves in the case of two prominent diseases. 

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3. Oral metagenomes from Native American Ancestors reveal distinct microbial lineages in the pre‐contact era

   https://doi.org/10.1002/ajpa.24735  

   Honap, Tanvi P.; Monroe, Cara R.; Johnson, Sarah J.; Jacobson, David K.; Abin, Christopher A.; Austin, Rita M.; Sandberg, Paul; Levine, Marc; Sankaranarayanan, Krithivasan; Lewis, Jr., Cecil M. (April 2023, American Journal of Biological Anthropology)

   Abstract ObjectivesLimited studies have focused on how European contact and colonialism impacted Native American oral microbiomes, specifically, the diversity of commensal or opportunistically pathogenic oral microbes, which may be associated with oral diseases. Here, we studied the oral microbiomes of pre‐contact Wichita Ancestors, in partnership with the Descendant community, The Wichita and Affiliated Tribes, Oklahoma, USA. Materials and MethodsSkeletal remains of 28 Wichita Ancestors from 20 archeological sites (dating approximately to 1250–1450 CE) were paleopathologically assessed for presence of dental calculus and oral disease. DNA was extracted from calculus, and partial uracil deglycosylase‐treated double‐stranded DNA libraries were shotgun‐sequenced using Illumina technology. DNA preservation was assessed, the microbial community was taxonomically profiled, and phylogenomic analyzes were conducted. ResultsPaleopathological analysis revealed signs of oral diseases such as caries and periodontitis. Calculus samples from 26 Ancestors yielded oral microbiomes with minimal extraneous contamination. Anaerolineaceae bacterium oral taxon 439 was found to be the most abundant bacterial species. Several Ancestors showed high abundance of bacteria typically associated with periodontitis such asTannerella forsythiaandTreponema denticola. Phylogenomic analyzes of Anaerolineaceae bacterium oral taxon 439 andT. forsythiarevealed biogeographic structuring; strains present in the Wichita Ancestors clustered with strains from other pre‐contact Native Americans and were distinct from European and/or post‐contact American strains. DiscussionWe present the largest oral metagenome dataset from a pre‐contact Native American population and demonstrate the presence of distinct lineages of oral microbes specific to the pre‐contact Americas. 

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4. Metagenomic analysis examines oral microbiome changes and interplay with immune response following prenatal total oral rehabilitation

   https://doi.org/10.1186/s12967-023-03997-9  

   Wu, Tong Tong; Sohn, Michael; Manning, Samantha; Beblavy, Robert; Gill, Steven; Quataert, Sally; Vasani, Shruti; Jang, Hoonji; Zeng, Yan; Bruno, Jennifer; et al (December 2023, Journal of Translational Medicine)

   Abstract BackgroundSuboptimal maternal oral health during pregnancy is potentially associated with adverse birth outcomes and increased dental caries risks in children. This study aimed to assess the oral microbiome and immune response following an innovative clinical regimen, Prenatal Total Oral Rehabilitation (PTOR), that fully restores women’s oral health to a “disease-free status” before delivery. MethodsThis prospective cohort study assessed 15 pregnant women at baseline and 3 follow-up visits (1 week, 2 weeks, and 2 months) after receiving PTOR. The salivary and supragingival plaque microbiomes were analyzed using metagenomic sequencing. Multiplexed Luminex cytokine assays were performed to examine immune response following PTOR. The association between salivary immune markers and oral microbiome was further examined. ResultsPTOR was associated with a reduction of periodontal pathogens in plaque, for instance, a lower relative abundance ofTannerella forsythiaandTreponema denticolaat 2 weeks compared to the baseline (p < 0.05). The alpha diversity of plaque microbial community was significantly reduced at the 1-week follow-up (p < 0.05). Furthermore, we observed significant changes in theActinomyces defective-associated carbohydrate degradation pathway andStreptococcus Gordonii-associated fatty acid biosynthesis pathway. Two immune markers related to adverse birth outcomes significantly differed between baseline and follow-up. ITAC, negatively correlated with preeclampsia severity, significantly increased at 1-week follow-up; MCP-1, positively correlated with gestational age, was elevated at 1-week follow-up. Association modeling between immune markers and microbiome further revealed specific oral microorganisms that are potentially correlated with the host immune response. ConclusionsPTOR is associated with alteration of the oral microbiome and immune response among a cohort of underserved US pregnant women. Future randomized clinical trials are warranted to comprehensively assess the impact of PTOR on maternal oral flora, birth outcomes, and their offspring’s oral health. 

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5. Ancient DNA and paleoproteomic analysis on Roman Imperial-era individuals from Histria, Romania

   https://doi.org/10.1016/j.jasrep.2024.104510  

   Wright, Sterling L; Rayfield, Kristen M; Singleton, Robin R; Hughes, Karissa; Soficaru, Andrei; Creţu, Ciprian; Huang, Lushuang; Wu, Si; Reinberger, Katherine L; Rabinowitz, Adam; et al (June 2024, Journal of Archaeological Science: Reports)

   Ancient biomolecules have become an increasingly important part of archaeological investigations interested in understanding population movements and health. Despite their ability to elucidate historically-attested contexts of human mobility and interaction between different cultural groups, biomolecular techniques are still underutilized in certain historical and archaeological contexts. One such context is the Roman Imperial limes, or border zone, along the lower reaches of the Danube, which saw more than five hundred years of migration, conflict, and accommodation among a wide range of populations, from Mediterranean settlers to steppe pastoralists. In this region, more than a century of archaeological investigation has unearthed the remains of tens of thousands of Roman-era individuals. However, only a limited number of contexts have undergone biomolecular analyses. While these deceased humans may offer an untapped reservoir of biomolecular information, many were collected during a period when the standard precautions and protocols for ancient biomolecular research were not yet established. Because contamination is a major barrier for successfully recovering ancient DNA and proteins, conducting a pilot study to assess bimolecular preservation of a small representative dataset of human remains before embarking on a more extensive research program may prevent unnecessary sampling. This study applies ancient DNA and paleoproteomic techniques to human remains from a Roman-period cemetery at Histria, a site located just south of the Danube at the edge of the Roman province of Moesia Inferior. The individuals from whom we sampled dentin and dental calculus were excavated between the 1940s and 1980s and were housed at the Francisc J. Rainer Institute since. Our results suggest that both microbial and human ancient DNA is preserved in the dental calculus and dentin samples. We also successfully recovered sex-specific amelogenin peptides in tooth enamel from three individuals, including a juvenile. In conclusion, our results are encouraging, signifying the feasibility of future aDNA and paleoproteomic research for this skeletal collection. Our analyses also showcase how sex estimation with genomic and proteomic methods may contradict traditional osteological approaches. These findings not only offer deeper insights into the lives of these individuals but also show promise for the investigation of broader anthropological questions, such as the impact of Roman annexation in this region. 

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