Understanding Ancient Microbiomes

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Environmental Microbiology".

Deadline for manuscript submissions: closed (31 July 2021) | Viewed by 19743

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Associate Professor, Western Australia Organic and Isotope Geochemistry Centre, School of Earth and Planetary Sciences, Curtin University, Bentley, WA 6102, Australia
Interests: sedimentary ancient DNA; paleomicrobiology; molecular paleoecology; paleobiogeochemical cycling; paleoenvironment; ocean health; Anthropocene
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Dear Colleagues, 

The rapidly expanding field of palaeomicrobiology—the study of ancient microorganisms—is perhaps best known for the sequencing and characterization of pathogenic bacterial, fungal, and viral agents from ancient human remains to reconstruct the history of diseases and the spread of human pandemics. Recently, ancient microbiomes are also being more widely analyzed in a variety of geologic records such as ice cores, permafrost-, peat-, and cave soils, as well as in lake and marine sediments.

The sequencing analysis of these ancient microbiomes can assist more traditional micropaleontological approaches in identifying the majority of microbial taxa that do not leave (easily) identifiable morphological remains in the fossil record and can, therefore, provide a more holistic overview of the evolution and interaction of past ecosystems such as in the context of paleoenvironmental and anthropogenic perturbations. The analysis of ancient microbiomes in the geologic record covers all domains of life: fungi and unicellular eukaryotes (protists), bacteria, archaea, bacteriophages, and protistal viruses. However, even if contamination with modern DNA can be ruled out, it can remain a challenge to determine what fraction of the microbiome in the environmental samples represents a true ancient signature from the time of death of the host organisms or from the time of burial in the geologic record. For example, subsurface bacteria (notably facultative and obligate anaerobes) are generally thought to be structured through in situ environmental conditions such as the availability of electron acceptors and donors, and soil or sediment porosity. However, recent studies suggest that a subset of subsurface microbial taxa were present at the time of deposition and that their vertical distribution in the geologic record was shaped by the paleoenvironmental conditions that prevailed at that time. For example, downcore sedimentary 16S rRNA gene profiling revealed that Holocene sediments of Laguna Potrok Lake (Argentina) reflected a vertical stratification linked to electron acceptors’ availability, while in the late Pleistocene, samples up to 50 Ka in age, salinity, organic matter, and the depositional conditions over the last Glacial–Interglacial cycle were the most important selective pressures. As another example, shotgun metagenomic analysis revealed subseafloor bacteria that were involved in denitrification during periods of oxygen minimum zone formation in the Arabian Sea. A switch to fermentation likely explains their long-term post-depositional survival. However, further development of robust molecular approaches and bioinformatics tools is required to determine to what extent ancient microbiomes represent dead, dormant, or metabolically active communities.

For this Special Issue, we invite you to send contributions on any aspects related to the study of ancient microbiomes covering all domains of life in ancient biological remains, as well as in all varieties of geologic records. For example, this could include studies ground-truthing the feasibility of subsurface microbiomes to provide long-term records of the paleodepositional environment and/or biogeochemical cycling in the context of shifts in paleoclimate or more recent anthropogenic perturbations.

text

Dr. Marco Coolen
Guest Editor

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Keywords

  • palaeomicrobiology
  • ancient DNA
  • biogeochemical cycling
  • palaeoclimate
  • Anthropocene
  • evolution of human diseases and pandemics

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Published Papers (5 papers)

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Research

20 pages, 2752 KiB  
Article
Mycobiome-Host Coevolution? The Mycobiome of Ancestral Human Populations Seems to Be Different and Less Diverse Than Those of Extant Native and Urban-Industrialized Populations
by Jelissa Reynoso-García, Yvonne Narganes-Storde, Tasha M. Santiago-Rodriguez and Gary A. Toranzos
Microorganisms 2022, 10(2), 459; https://doi.org/10.3390/microorganisms10020459 - 16 Feb 2022
Cited by 4 | Viewed by 3653
Abstract
Few data exist on the human gut mycobiome in relation to lifestyle, ethnicity, and dietary habits. To understand the effect of these factors on the structure of the human gut mycobiome, we analyzed sequences belonging to two extinct pre-Columbian cultures inhabiting Puerto Rico [...] Read more.
Few data exist on the human gut mycobiome in relation to lifestyle, ethnicity, and dietary habits. To understand the effect of these factors on the structure of the human gut mycobiome, we analyzed sequences belonging to two extinct pre-Columbian cultures inhabiting Puerto Rico (the Huecoid and Saladoid) and compared them to coprolite samples found in Mexico and Ötzi, the Iceman’s large intestine. Stool mycobiome samples from extant populations in Peru and urban cultures from the United States were also included. The ancient Puerto Rican cultures exhibited a lower fungal diversity in comparison to the extant populations. Dissimilarity distances showed that the Huecoid gut mycobiome resembled that from ancient Mexico. Fungal genera including Aspergillus spp., Penicillium spp., Rasamsonia spp., Byssochlamys spp., Talaromyces spp., Blastomyces spp., Monascus spp., and Penicilliopsis spp. were differentially abundant in the ancient and extant populations. Despite cultural differences, certain fungal taxa were present in all samples. These results suggest that culture and diet may impact the gut mycobiome and emphasize that modern lifestyles could be associated with the alteration of gut mycobiome diversity. The present study presents data on ancient and extant human gut mycobiomes in terms of lifestyle, ethnicity, and diet in the Americas. Full article
(This article belongs to the Special Issue Understanding Ancient Microbiomes)
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17 pages, 2084 KiB  
Article
Molecular and Pigment Analyses Provide Comparative Results When Reconstructing Historic Cyanobacterial Abundances from Lake Sediment Cores
by Maïlys Picard, Susanna A. Wood, Xavier Pochon, Marcus J. Vandergoes, Lizette Reyes, Jamie D. Howarth, Ian Hawes and Jonathan Puddick
Microorganisms 2022, 10(2), 279; https://doi.org/10.3390/microorganisms10020279 - 25 Jan 2022
Cited by 10 | Viewed by 3714
Abstract
Understanding the historical onset of cyanobacterial blooms in freshwater bodies can help identify their potential drivers. Lake sediments are historical archives, containing information on what has occurred in and around lakes over time. Paleolimnology explores these records using a variety of techniques, but [...] Read more.
Understanding the historical onset of cyanobacterial blooms in freshwater bodies can help identify their potential drivers. Lake sediments are historical archives, containing information on what has occurred in and around lakes over time. Paleolimnology explores these records using a variety of techniques, but choosing the most appropriate method can be challenging. We compared results obtained from a droplet digital PCR assay targeting a cyanobacterial-specific region of the 16S rRNA gene in sedimentary DNA and cyanobacterial pigments (canthaxanthin, echinenone, myxoxanthophyll and zeaxanthin) analysed using high-performance liquid chromatography in four sediment cores. There were strong positive relationships between the 16S rRNA gene copy concentrations and individual pigment concentrations, but relationships differed among lakes and sediment core depths within lakes. The relationships were more consistent when all pigments were summed, which we attribute to different cyanobacteria species, in different lakes, at different times producing different suites of pigments. Each method had benefits and limitations, which should be taken into consideration during method selection and when interpreting paleolimnological data. We recommend this biphasic approach when making inferences about changes in the entire cyanobacterial community because they yielded complementary information. Our results support the view that molecular methods can yield results similar to traditional paleolimnological proxies when caveats are adequately addressed. Full article
(This article belongs to the Special Issue Understanding Ancient Microbiomes)
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20 pages, 4468 KiB  
Article
From Water into Sediment—Tracing Freshwater Cyanobacteria via DNA Analyses
by Ebuka Canisius Nwosu, Patricia Roeser, Sizhong Yang, Lars Ganzert, Olaf Dellwig, Sylvia Pinkerneil, Achim Brauer, Elke Dittmann, Dirk Wagner and Susanne Liebner
Microorganisms 2021, 9(8), 1778; https://doi.org/10.3390/microorganisms9081778 - 21 Aug 2021
Cited by 16 | Viewed by 4349
Abstract
Sedimentary ancient DNA-based studies have been used to probe centuries of climate and environmental changes and how they affected cyanobacterial assemblages in temperate lakes. Due to cyanobacteria containing potential bloom-forming and toxin-producing taxa, their approximate reconstruction from sediments is crucial, especially in lakes [...] Read more.
Sedimentary ancient DNA-based studies have been used to probe centuries of climate and environmental changes and how they affected cyanobacterial assemblages in temperate lakes. Due to cyanobacteria containing potential bloom-forming and toxin-producing taxa, their approximate reconstruction from sediments is crucial, especially in lakes lacking long-term monitoring data. To extend the resolution of sediment record interpretation, we used high-throughput sequencing, amplicon sequence variant (ASV) analysis, and quantitative PCR to compare pelagic cyanobacterial composition to that in sediment traps (collected monthly) and surface sediments in Lake Tiefer See. Cyanobacterial composition, species richness, and evenness was not significantly different among the pelagic depths, sediment traps and surface sediments (p > 0.05), indicating that the cyanobacteria in the sediments reflected the cyanobacterial assemblage in the water column. However, total cyanobacterial abundances (qPCR) decreased from the metalimnion down the water column. The aggregate-forming (Aphanizomenon) and colony-forming taxa (Snowella) showed pronounced sedimentation. In contrast, Planktothrix was only very poorly represented in sediment traps (meta- and hypolimnion) and surface sediments, despite its highest relative abundance at the thermocline (10 m water depth) during periods of lake stratification (May–October). We conclude that this skewed representation in taxonomic abundances reflects taphonomic processes, which should be considered in future DNA-based paleolimnological investigations. Full article
(This article belongs to the Special Issue Understanding Ancient Microbiomes)
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21 pages, 2521 KiB  
Article
Sedimentary Ancient DNA (sedaDNA) Reveals Fungal Diversity and Environmental Drivers of Community Changes throughout the Holocene in the Present Boreal Lake Lielais Svētiņu (Eastern Latvia)
by Liisi Talas, Normunds Stivrins, Siim Veski, Leho Tedersoo and Veljo Kisand
Microorganisms 2021, 9(4), 719; https://doi.org/10.3390/microorganisms9040719 - 31 Mar 2021
Cited by 15 | Viewed by 3732
Abstract
Fungi are ecologically important in several ecosystem processes, yet their community composition, ecophysiological roles, and responses to changing environmental factors in historical sediments are rarely studied. Here we explored ancient fungal DNA from lake Lielais Svētiņu sediment throughout the Holocene (10.5 kyr) using [...] Read more.
Fungi are ecologically important in several ecosystem processes, yet their community composition, ecophysiological roles, and responses to changing environmental factors in historical sediments are rarely studied. Here we explored ancient fungal DNA from lake Lielais Svētiņu sediment throughout the Holocene (10.5 kyr) using the ITS metabarcoding approach. Our data revealed diverse fungal taxa and smooth community changes during most of the Holocene with rapid changes occurring in the last few millennia. More precisely, plankton parasitic fungi became more diverse from the Late Holocene (2–4 kyr) which could be related to a shift towards a cooler climate. The Latest Holocene (~2 kyr) showed a distinct increase in the richness of plankton parasites, mycorrhizal, and plant pathogenic fungi which can be associated with an increased transfer rate of plant material into the lake and blooms of planktonic organisms influenced by increased, yet moderate, human impact. Thus, major community shifts in plankton parasites and mycorrhizal fungi could be utilized as potential paleo-variables that accompany host-substrate dynamics. Our work demonstrates that fungal aDNA with predicted ecophysiology and host specificity can be employed to reconstruct both aquatic and surrounding terrestrial ecosystems and to estimate the influence of environmental change. Full article
(This article belongs to the Special Issue Understanding Ancient Microbiomes)
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19 pages, 2760 KiB  
Article
Landscape Setting Drives the Microbial Eukaryotic Community Structure in Four Swedish Mountain Lakes over the Holocene
by Eric Capo, Sofia Ninnes, Isabelle Domaizon, Stefan Bertilsson, Christian Bigler, Xiao-Ru Wang, Richard Bindler and Johan Rydberg
Microorganisms 2021, 9(2), 355; https://doi.org/10.3390/microorganisms9020355 - 11 Feb 2021
Cited by 6 | Viewed by 3014
Abstract
On the annual and interannual scales, lake microbial communities are known to be heavily influenced by environmental conditions both in the lake and in its terrestrial surroundings. However, the influence of landscape setting and environmental change on shaping these communities over a longer [...] Read more.
On the annual and interannual scales, lake microbial communities are known to be heavily influenced by environmental conditions both in the lake and in its terrestrial surroundings. However, the influence of landscape setting and environmental change on shaping these communities over a longer (millennial) timescale is rarely studied. Here, we applied an 18S metabarcoding approach to DNA preserved in Holocene sediment records from two pairs of co-located Swedish mountain lakes. Our data revealed that the microbial eukaryotic communities were strongly influenced by catchment characteristics rather than location. More precisely, the microbial communities from the two bedrock lakes were largely dominated by unclassified Alveolata, while the peatland lakes showed a more diverse microbial community, with Ciliophora, Chlorophyta and Chytrids among the more predominant groups. Furthermore, for the two bedrock-dominated lakes—where the oldest DNA samples are dated to only a few hundred years after the lake formation—certain Alveolata, Chlorophytes, Stramenopiles and Rhizaria taxa were found prevalent throughout all the sediment profiles. Our work highlights the importance of species sorting due to landscape setting and the persistence of microbial eukaryotic diversity over millennial timescales in shaping modern lake microbial communities. Full article
(This article belongs to the Special Issue Understanding Ancient Microbiomes)
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