Written by Daniel Colman (Guest Editor, Montana State University), Ruth Blake (Guest Editor, Yale University) and Hanna Landenmark (Associate Editor, PLOS ONE). We are delighted to introduce a Collection entitled Life in Extreme Environments, consisting
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Introducing the Life in Extreme Environments Collection
Written by Daniel Colman (Guest Editor, Montana State University), Ruth Blake (Guest Editor, Yale University) and Hanna Landenmark (Associate Editor, PLOS ONE). We are delighted to introduce a Collection entitled Life in Extreme Environments, consisting
Introducing the Life in Extreme Environments Collection
Written by Daniel Colman (Guest Editor, Montana State University), Ruth Blake (Guest Editor, Yale University) and Hanna Landenmark (Associate Editor, PLOS ONE).
We are delighted to introduce a Collection entitled Life in Extreme Environments, consisting of papers published in PLOS Biology and PLOS ONE. This interdisciplinary Collection helps us better understand the diversity of life on Earth in addition to the biological processes, geochemistry, and nutrient cycling taking place in many of the Earth’s most inhospitable environments, while also enabling us to make inferences about the potential for life beyond Earth. Microorganisms and other life in extreme environments are fundamental agents of geochemical and nutrient cycling in many of the most poorly understood environments on Earth. While we tend to think of these environments as lying at the boundaries of what life is capable of dealing with, many organisms are uniquely adapted to thrive in habitats at the extremes of temperatures, pressures, water availability, salinity, and other environmental characteristics. Indeed, these environments are certainly not “extreme” to these organisms, but represent their unique niches within ecosystems on Earth. The papers included in this Collection bring together research from different disciplines including the biosciences, geosciences, planetary sciences, and oceanography in order to shed light on this crucial topic.
We are immensely grateful to our Guest Editor team- Paola Di Donato (Università degli Studi di Napoli “Parthenope”), Jiasong Fang (Hawaii Pacific University), David Pearce (Northumbria University), Anna Metaxas (Dalhousie University), Henrik Sass (Cardiff University), Ruth Blake (Yale University), Daniel Colman (Montana State University), Karen Olsson-Francis (The Open University), Frank Reith (The University of Adelaide), Felipe Gómez (Centro de Astrobiología, Instituto Nacional de Técnica Aeronáutica)- for curating this Collection.
The importance of studying life in extreme environments
It is important to study life in extreme environments in order to establish life’s limits – both physical and geographic (e.g., the depth of life beneath the seafloor), as well as the capacity of life to withstand and adapt to change. Besides significantly expanding our understanding of the limits of familiar and extreme life on Earth, studies in extreme environments have also revised our understanding of the nature of the earliest life on our planet, as well as providing the possibility of discovering new industrially useful organisms or biological products. Moreover, if there is life on other planetary bodies in our solar system or elsewhere, they will almost certainly be living in what we consider “extreme environments” on Earth. Thus, understanding how life copes with what we consider extreme conditions can provide insight into how life may be able to persist on other planetary bodies, perhaps in the subsurface oceans of Saturn’s moon, Enceladus, or Jupiter’s moon, Europa.
Investigating extreme life
One of the most exciting aspects of researching extreme life is the exploration of the unknown and discovery of new things in unexpected places that expands our very way of thinking. Microbial life, in particular, has evolved to find a way to exist and even thrive pretty much everywhere we have looked so far. Moreover, contemporary research of extremophiles is happening at an exciting time when the lines between scientific fields have been increasingly blurred. The more we understand about how environments not only influence life in extreme environments, but how life also influences those environments, the more apparent it becomes that extreme ecosystems are dynamic systems with feedback between biological activities and ecosystem properties. These interdisciplinary perspectives certainly invigorate the study of extreme life.
Extremophile research is often interdisciplinary by nature, perhaps due to the close association with biological organisms and their ecosystems, and thus the need to consider environmental, geologic, ecological, physiological, and even evolutionary considerations when investigating how organisms are able to push the limits of life. The challenges can be considerable due to the need to integrate across many disciplines, which requires expertise in a number of areas (and requiring scientists across disciplines to productively engage one another). But the reward for conducting this type of research is that it can transform how we view the relationships between living organisms and their environments. These insights can be profound in terms of our understanding of organismal biology and broader evolutionary processes of adaptation.
Yet, by their very nature, extreme environments pose significant challenges for studying biological life within them. This can be due to their remote locations (e.g., deep sea environments, high altitude environments), or to specific dangers associated with studying them (e.g., geothermal fields or other volcanic environments). Indeed, the reason that these environments are considered “extreme” is because they are not amenable to humans spending much time within them. It takes serious dedication and preparation to execute scientific research under such conditions.
The future of extremophile research
The last 30-40 years have reshaped our understanding of life in extreme environments, but much remains to be discovered. As one example, we’re still only beginning to understand what types of microbial life can exist in extreme environments, let alone what the physiological adaptations of these organisms might be. One of the greatest questions in the study of life in extreme environments i whether life is present in other “extreme environments” of the Universe beyond our planet. While we cannot know whether answers to this question will be forthcoming in the near future, great strides are being made in pointing us in what may be the most likely directions.
The Life in Extreme Environments Collection
This Collection showcases a wide variety of research on how life, from microorganisms like bacteria, archaea, diatoms, and algae, through to macroorganisms like humans, survive and flourish in diverse extreme environments, ranging from hydrothermal vents and the deep ocean to permafrosts and hypersaline lakes, and from the high Andes to deep space. Many papers illustrate highly interdisciplinary approaches and collaborations, and provide important insights into the limits of life on Earth in truly extreme environments. As indicated above, extremophiles provide insight into far-ranging topics like the limits of life on Earth, biogeochemical cycling in extreme but globally important environments, insights into early life on Earth, and how organisms cope with conditions that push the boundaries of organismal physiology.
A critical component of extremophile research is understanding how extremophiles are distributed across environments in both contemporary settings as well as over geologic time. Serpentinizing environments are considered to be analogs for the environments where life originated on Earth (and that may also support life on other planetary bodies). The investigation of fully serpentinized rocks by Khilyas et al. document the endolithic (i.e., within-rock dwelling) microbial diversity within these unique environments, their associations with their mineral environments, and contrast their findings with those of active serpentinizing aqueous environments. Such studies examining the connection between extreme environments and their native microbiomes can be critical for understanding how organisms have and continue to interact with their environments over time. Another study in the Collection by Kiel and Peckmann provides new insights into the association of macrofauna with hydrothermal vents over the past ~550 million years. Their survey of dominant brachiopod and bivalve fossils over this period challenge the pre-existing hypotheses that these two groups competed for the same resources, with the latter group ultimately gaining prominence in the last ~100 million years. However, the authors show that the two groups likely inhabited different vent environments altogether, with brachiopods inhabiting hydrocarbon seeps and bivalves preferring sulfide-producing vents in association with their symbiotic sulfide oxidizing bacteria. To better understand the contemporary distributions of important marine microorganisms, Ferreira da Silva et al. documented how diatom communities are associated with macroalgae in the waters near the South Shetland Islands of Antarctica, revealing a potential role of the unique Antarctic climate in determining the biogeography of diatoms and their associated macroalgae. Indeed, the relationships among organisms may be critical for the habitation of extreme environments. In another investigation of cross-taxa associations in extreme environments, Gallet et al. evaluated the diversity of microbiota associated with enigmatic bioluminescent lantern fish species, and found that the latter might interact with its microbiome to inhabit the extreme environment of deep southern oceans. The data provide a better understanding of these important associations in key species involved in the ecosystem function of extreme deep sea environments.
Although extreme environments are often considered marginal habitats of mostly local influence, the functions of some extreme environments, and the organisms inhabiting them, can have particularly important implications for global biogeochemical cycling. For example, Nayak et al. document new insights into the functioning of one of the most important microbial enzymes involved in global carbon cycling, the methyl-coenzyme M reductase protein of methanogens, which catalyzes the key step of methanogenesis allowing the biological production of methane, which contributes to a significant portion of global methane production. In the authors’ investigation, they show how the protein is post-translationally modified by a previously unknown mechanism, and that this ‘tuning’ of methyl-coenzyme M reductase has profound impacts on the adaptation of methanogens to various environmental conditions. Anoxic peatlands are one such environment where methanogens play critical roles in biogeochemical cycling. These anoxic peatland environments are extreme environments that are important for global biogeochemical cycling, despite only occupying a small fraction of the total land space. Kluber et al. used an experimental warming approach to investigate how deep, anoxic peatland reserves would respond to fluctuating environmental conditions. The authors document that temperature is a key parameter that could drastically affect the decomposition of peatland nutrient stocks and their contribution to global biogeochemical cycling.
Key to the interaction between organisms and extreme environments are the adaptations that extreme environments impose upon organisms. The Collection features a number of investigations documenting the unique adaptations of microorganisms and macroorganisms to habitats ranging from hydrothermal vents to space at both the genomic and physiological levels. One of the most enigmatic discoveries of extreme environments over the past half century was the identification of entire ecosystems that dwell on or around hydrothermal vents at the ocean floor that are sustained by inorganic chemical synthesis from hydrothermal vent fluid chemicals. The paper within this Collection by Zhu et al. provides new evidence for the genetic mechanisms that allow the habitation of vent ecosystems by two distinct shrimp species that characteristically inhabit different thermal regions of vents. Using transcriptomic approaches, the authors identified new molecular mechanisms underlying how macrofauna can adapt to different hydrothermal niches within these extreme systems. Likewise, Díaz-Riaño et al. used transcriptomics to identify the mechanisms of ultraviolet radiation resistance (UVR) within high UVR bacterial strains that were isolated from high altitudes within the Colombian Andes. These new insights provide much needed resolution into the RNA-based regulatory mechanisms underlying UVR in organisms, which represents a fundamental knowledge-gap in our understanding of organismal adaptations to extreme altitude environments.
While life that persists continuously under extreme environments provide valuable information to understand the physiological limits of life, it is also critical to understand how life adapted to more ‘normal’ environments can withstand excursions to extreme environments over prolonged periods of time. One such example are oxygen minimum zones that occur in deep oceans where oxygen levels have been depleted to levels thought to not be able to support higher life, in what is termed ‘hypoxic conditions’. Nevertheless, some higher organisms are capable of living in such environments, although their adaptations to this lifestyle are not currently clear. One such species is the bluntnose sixgill shark that can tolerate very low levels of oxygen. Using an array of biologging techniques that allowed them to monitor the physiological and behavioral activities of these sharks, Coffey et al. provide evidence for their migratory behavior and long periods of exposure to hypoxic conditions in the deep sea. In addition to elucidating how sixgill sharks cope with extreme deep sea conditions, the new ecophysiological logging techniques provide a new platform for future studies of organisms adapted to the extremes of deep oceans. Among the possible excursions of life to extreme environments, none are potentially more problematic than the travel of humans to space. A common physiological effect of space transit is the bone mineral density (BMD) loss that is experienced by astronauts. In a paper within the Collection, Axpe et al., performed a modeling analysis based on BMD loss by previous astronauts involved in long-term missions in order to evaluate the potential for these harmful effects on trips that might become targets for longer manned missions to Mars or elsewhere. The study thus provides critical new data to inform these important missions.
As exemplified by the papers within this Collection, unique adaptations allow life to persist in extreme environments. These adaptations can also be useful in biotechnological applications, as several other papers in the Collection demonstrate. Halophiles that inhabit extremely saline environments have long been a source for bioprospecting due to their unique adaptations that allow them to maintain osmotic balance within environments that most types of life could not survive in. Notably, halophiles often concentrate unique biomolecules in order to overcome the abiotic stress of hypersaline environments. In their manuscript, Abdollahnia et al. explore the previously little-investigated ability of halophiles to concentrate nanoparticles, finding evidence for the unique ability to concentrate metal nanoparticles within archaeal and bacterial species. Importantly, these organisms could represent a potential environmentally-friendly means of synthesizing unique metal nanoparticles. Thus, the identification of new bio-resources is an area of ongoing and intense interest in the investigation of extreme life.
As is evident by the diverse range of topics, organisms, and environments within the papers of this Collection, the investigation of extreme life incorporates numerous fields of study and a wealth of methods to understand the limits to life on Earth. We’ll be adding new papers to the Collection as they are published, so please do keep checking back.
About the Guest Editors
Ruth Blake
Ruth Blake is a Professor in the departments of Geology & Geophysics and Environmental Engineering, and in the School of Forestry & Environmental Studies at Yale University. Dr. Blake’s areas of expertise include marine biogeochemistry, stable isotope geochemistry and geomicrobiology. Her recent work focuses on developing new stable isotope tools, geochemical proxies and biomarkers to study marine/microbial phosphorus cycling and evolution of the phosphorus cycle from pre-biotic to recent.
Dr. Blake is engaged in a range of studies on co- evolution of earth and life and the impacts of both on biogeochemical processes occurring in the oceans, deep-sea sediments, seafloor hydrothermal systems and the sub-seafloor deep biosphere. Dr. Blake has participated in several ocean exploration/ research expeditions including cruises to: FeMO observatory at Loihi undersea volcano, 9°N EPR, Orca Basin in the Gulf of Mexico and North Pond in the mid-Atlantic. She has also served as shipboard scientist on Ocean Drilling Program and R/V Atlantis /DSV ALVIN platforms. Ruth Blake graduated from the University of Michigan in 1998 with a PhD in geochemistry.
Daniel Colman
Dan is currently an assistant research professor at Montana State University and is an environmental microbiologist with primary research interests in broadly understanding how microbial populations interact with one another and with their environments. To investigate these broad topics, he uses a suite of interdisciplinary techniques at the intersection of environmental microbiology, biogeochemistry, geomicrobiology, microbial physiology, geochemistry, hydrology, and microbial evolution.
In particular, his work leverages environmental genomics methods coupled to in situ and laboratory experiments along with geochemical insights from hydrological and geochemical analyses to understand 1) how and why environments structure micobial communities, 2) how microbial communities shape their environments, and 3) how environments and microbial populations have co- evolved through time. In particular, he has largely focused on evaluating these questions in extreme environments, and especially hydrothermal systems, which represent an excellent platform to deconvolute microbial-environment relationships across substantial environmental gradients.
Paola Di Donato
Graduated in Chemistry, Paola received her PhD in 2002 and since 2008 she is a Researcher in Biochemistry at the Department of Science and Technology of University of Naples “Parthenope”; in 2016 she has been appointed as the Dean’s delegate to managing the Institutional Repository of the University “Parthenope”.
Her research interests are the valorisation of waste vegetable biomass and the study of extremophilic bacteria. With regard to the first topic, her research focuses on the recovery of value added chemicals (polysaccharides and polyphenols) and the production of energy (bioethanol) from wastes of vegetables food industry and of dedicated crops (giant reed, cardoon). With regard to the study of extremophilic bacteria, her research activity is aimed at studying the biotechnologically useful biomolecules (enzymes and exopolysaccharides) produced by these bacteria; in the last seven years, particular attention has been paid to the study of extremophiles in relation to Astrobiology, the multidisciplinary approach to the study of origin and evolution of life on Earth and in the Universe.
Felipe Gómez
Dr. Felipe Gómez is a senior staff scientist at the CAB. His research work focuses on the study of extreme environments, limits of life and, by extrapolation, development of habitability potential in adverse environments. He participates in Mars exploration space missions to search for traces of life and study the habitability potential of the red planet. He is currently part of the scientific team (Co-Investigator) of the Rover Environmental Monitoring Station (REMS) instrument aboard the NASA Curiosity-MSL rover that is studying the surface of Mars at this time. Dr. Felipe Gómez is Co-I of MEDA instrument that will be onboard Mars2020 NASA mission to Mars.
He has been part of the scientific team of several campaigns of astrobiological interest in studying different extreme environments. The project M.A.R.T.E. (Mars Analogue Research and Technology Development) began in 2003 and extended until 2006. Its principal investigator was Dr. Carol Stocker of NASA Ames Research Center. This project was funded by NASA within NASA’s ASTEP program for the development of technology for future space missions. This project was developed with the collaboration of several institutions in the United States and CAB. It consisted in the study of the subterranean environment of the zone of origin of the Tinto River (Huelva) where several perforations were made (160 m deeper) until reaching the anoxic zone isolated from the surface. The ultimate goal of the project was the design and development of an automatic platform for drilling without direct human intervention (automatic drilling) on ??the surface of Mars. This project was the beginning of research into the development of automatic drilling instruments for this purpose. It was developed in three phases: first and second year with non-automatic perforations and “in situ” study of the samples that were obtained in real time. In the third year, the automatic platform was implemented.
Jiasong Fang
Jiasong Fang is a professor in the College of Natural and Computational Sciences of Hawaii Pacific University, Distinguished Chair Professor in the College of Marine Sciences of Shanghai Ocean University, and Director of the Shanghai Engineering Research Center of Hadal Science and Technology. Dr. Fang received his Ph.D. in oceanography from Texas A&M University and did his postdoctoral training at the Department of Microbiology of Miami University.
His scientific interests are primarily in the areas of high-pressure microbiology and biogeochemistry, focusing on piezophilic microorganisms and their role in mediating biogeochemical cycles in the deep ocean and the deep biosphere. He has co-authored 100 scientific publications.
Anna Metaxas
Dr. Anna Metaxas is a Professor in Oceanography at Dalhousie University. She received a B.Sc. in Biology from McGill University in 1986, a MSc in Oceanography from the University of British Columbia in 1989 and a PhD from Dalhousie University in 1994. She was a Postdoctoral Fellow at Harbor Branch Oceanographic Institution from 1995 to 1997, and a Postdoctoral Scholar at Woods Hole Oceanographic Institution from 1997 to 1999.
Her research focuses on the factors that regulate populations of benthic marine invertebrates, particularly early in their life history. She uses a combination of approaches, such as field sampling, laboratory experiments and mathematical modelling, to study organisms of ecological and economic importance, including invasive species. She has worked in a variety of habitats from shallow rocky subtidal regions to the deep-sea, including hydrothermal vents and deep- water corals, in temperate and tropical regions of the world. Her research has implications for marine conservation, such as the establishment and success of conservation areas for benthic populations.
Karen Olsson-Francis
Dr. Karen Olsson-Francis is a Senior Lecturer at the Open University, in the United Kingdom. Her research focuses on understanding the role that microorganisms play in biogeochemical cycling in extreme environments. She is interested in this from a diversity and functional prospective. In particular, she has focused on studying terrestrial analogue sites and utilizing this information to understand how, and where, potential evidence of life can be found elsewhere in the Solar System.
David Pearce
The underlying theme of David Pearce’s research is to use microbiology (and in particular novel molecular techniques applied to microbial ecology, microbial biodiversity and activity, environmental genomics, biogeochemical cycling and model extremophiles) to understand Polar ecosystem function and the potential for shifts in biogeochemical activity that may result from environmental change. He has taken the lead in the development of new frontiers of research in metagenomics, chemosynthetic communities, sediment sequestration of carbon and subglacial lake environments and have initiated new interdisciplinary approaches on the aerial environment (with chemists), ice nucleation activity (with physicists) and in the biogeochemistry of ice (with glaciologists).
Frank Reith
Frank Reith is an Associate Professor in geomicrobiology at the School of Biological Sciences at University of Adelaide and CSIRO Land and Water, where he heads the Microbes and Heavy Metal Research Group. He holds a PhD in Earth Sciences from the Australian National University. He is interested in microbial processes that affect metal cycling and the formation of new minerals. In turn, he also studies how microbes are affected by elevated concentrations of heavy metals in extreme environments. His particular interests lie in the biomediated cycling of noble/heavy metals, e.g., gold, silver, platinum, uranium, osmium and iridium.
An important aim of the fundamental processes understanding created by his research is to use it to develop tools for industry, e.g., biosensors and bioindicators for mineral exploration, as well as biotechnological methods for mineral processing and resource recovery from electronic waste. Thereby, his approach is highly multidisciplinary and covers field expeditions to remote corners of the Earth, synchrotron research, meta-genomic and proteomic approaches as well as statistical-, geochemical- and reactive transport modelling.
We were very saddened to hear of Frank’s passing before this Collection published. We are immensely grateful for his contributions to PLOS and to his field of research, as well as for his enthusiasm and kindness. Our thoughts go out to his family and friends.
Henrik Sass
Dr. Henrik Sass is senior lecturer in Geomicrobiology at the School of Earth and Ocean Sciences of Cardiff University. He received his PhD from the University of Oldenburg (Germany).
Henrik is a biogeochemist, geomicrobiologist and microbial physiologist with a special interest in anaerobic processes and the prokaryotes involved, such as the strictly anaerobic sulphate reducers and methanogens. He has been working on anaerobic metabolism and described new metabolic pathways in methanogens. One main topic of his research is life in the extreme environments, particularly life in the deep biosphere and in deep-sea anoxic brine lakes. These studies aim to reveal how anaerobes adapt to their particular ecological niches (e.g. oxygen tolerance of sulphate reducers). His work utilizes a range of different approaches including in situ activity measurements and the estimation of viable population sizes, but also culture-based laboratory experiments. Another aspect of his work has been the use of biomarkers, including dipicolinic acid for the detection of endospores in environmental samples.
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Sharing is Caring: Varied Diets in Dinosaurs Promoted Coexistence
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Modern Humans: Were We Really Better than Neanderthals, or Did We Just Get Lucky?
We’ve all heard the story: dim-witted Neanderthals couldn’t quite keep up with our intelligent modern human ancestors, leading to their eventual downfall and disappearance from the world we know now. Apparently they needed more brain space for their eyes. The authors of a recent PLOS ONE paper are digging into the ideas behind this perception, and take a closer look at eleven common hypotheses for the demise of the Neanderthals, comparing each to the latest research in this field to convince us that Neanderthals weren’t the simpletons we’ve made them out to be.
The authors tackled ideas like the Neanderthal’s capacity for language and innovative ability, both often described as possible weaknesses leading to their decline. Analyzing the published research on each topic, they found that archaeologists often used their finds to “build scenarios” that agreed with the running theories of human superiority, and that some long-held truths have now been challenged by recent discoveries and ongoing research at the same excavation sites.
As one example, researchers who found shell beads and pieces of ochre and manganese in South Africa—used as pigments—claimed them as evidence of the use of structured language in anatomically modern humans. While we can only guess when linking items like these to the presence of language, new findings at Neanderthal sites indicate that they also decorated objects with paints and created personal ornaments using feathers and claws. Whatever the anatomically modern humans were doing in South Africa, Neanderthals were also doing in Europe around the same time, negating the claim that this ability may have provided the anatomically modern humans with better survival prospects once they arrived in Europe.
Another set of South African artifacts led the archaeological community to believe that anatomically modern humans were capable of rapidly improving on their own technology, keeping them ahead of their Neanderthal contemporaries. Two generations of tools, created during the Stillbay and Howiesons Poort periods, were originally believed to have evolved in phases shorter than 10,000 years—a drop in the bucket compared to the Neanderthals’ use of certain tools, unchanged, for 200,000 years. However, new findings suggest that the Stillbay and Howiesons Poort periods lasted much longer than previously thought, meaning that the anatomically modern humans may not have been the great visionaries we had assumed. Additionally, while Neanderthals were not thought capable of crafting the adhesives used by anatomically modern humans to assemble weapons and tools, it is now known that they did, purifying plant resin through an intricate distillation process.
We’re all living proof that anatomically modern humans survived in the end. Perhaps in an effort to flatter our predecessors, we have been holding on to dated hypotheses and ignoring recent evidence showing that Neanderthals were capable of a lot more (and perhaps the anatomically modern humans of a lot less) skill-wise than previously believed. Genetic studies continue to support the idea that anatomically modern humans and Neanderthals interbred and show that the genome of modern humans with Asian or European ancestry contains nearly 2% Neanderthal genes, a substantial quantity considering 40,000 years and 2000 generations have passed since they ceased to exist. These genes may have helped modern humans adjust to life outside of Africa, possibly aiding in the development of our immune system and variation in skin color. Researchers believe that the concentration of Neanderthal genes in modern humans was once much higher, but genetic patterns in modern humans show that hybrid Neanderthal-Human males may have been sterile, leaving no opportunity for their genes to be passed to the next generation.
So, while they may not walk among us today, we have Neanderthals to thank for some major adaptations that allowed us to thrive and spread across the planet. Too bad they’re not here to see the wonderful things we were able to accomplish with their help.
Related links:
Picked Clean: Neanderthals’ Use of Toothpicks to Fight Toothache
Sharing was Caring for Ancient Humans and Their Prehistoric Pups
Citation: Villa P, Roebroeks W (2014) Neandertal Demise: An Archaeological Analysis of the Modern Human Superiority Complex. PLoS ONE 9(4): e96424. doi:10.1371/journal.pone.0096424
Image 1: Neandertaler im Museum from Wikimedia Commons
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For Yeast’s Sake: The Benefits of Eating Cheese, Chocolate, and Wine
Yeast—including more than 1500 species that make up 1% of all known fungi—plays an important role in the existence of many of our favorite foods. With a job in everything from cheese making to alcohol production to cocoa preparation, humans could not produce such diverse food products without this microscopic, unicellular sous-chef. While we have long been aware of our dependence on yeast, new research in PLOS ONE suggests that some strains of yeast would not be the same without us, either.
Studies have previously shown how our historical use of yeast has affected the evolution of one of the most commonly used species, Saccharomyces cerevisiae, creating different strains that are used for different purposes (bread, wine, and so on). To further investigate our influence on yeast, researchers from the University of Bordeaux, France, took a look at a different yeast species of recent commercial interest, Torulaspora delbrueckii. In mapping the T. delbrueckii family tree, the authors show not only that human intervention played a major role in the shaping of this species, but they provide us with valuable information for further improving this yeast as a tool for food production.
The authors collected 110 strains of T. delbrueckii from global sources of wine grapes, baked goods, dairy products, and fermented beverages. Possible microsatellites, or repeating sequences of base pairs (like A-T and G-C), were found in one strain’s DNA and used to create tools that would identify similar sequences in the other strains. They used the results to pinpoint eight different microsatellite markers (base pair sequences) that were shared by some strains but not others to measure genetic variation in the T. delbrueckii family. The composition of each strain was measured using microchip electrophoresis, a process in which DNA fragments migrate through a gel containing an electric field, which helps researchers separate the fragments according to size. As each strain’s microsatellite markers were identified, the information was added to a dendrogram (a funny-looking graph, shown below) to illustrate the level of similarity between strains. The researchers also estimated the time it took different strains to evolve by comparing the average rate of mutation and reproduction time for T. delbrueckii to the level of genetic difference between each strain.
The dendrogram shows four clear clusters of yeast strains heavily linked to each sample’s origin. Two groups contain most of the strains isolated from Nature, but can be distinguished from each other by those collected on the American continents (nature Americas group) and those collected in Europe, Asia, and Africa (nature Old World group). The other two clusters include strains collected from food and drink samples, but cannot be discriminated by geographic location. The grape/wine group contains 27 strains isolated from grape habitats in the major wine-producing regions of the world: Europe, California, Australia, New Zealand, and South America. The bioprocess group contains geographically diverse strains collected from other areas of food processing—such as bread products, spoiled food, and fermented beverages—and includes a subgroup of strains used specifically for dairy products. Further analysis of the variation between strains confirmed that, while the clusters don’t perfectly segregate the strains according to human usage, and geographic origin of the sample played some role in diversity, a large part of the population’s structure is explained by the material source of the strain.
Divergence times calculated for the different groups further emphasize the connection between human adoption of T. delbrueckii yeast and the continued evolution of this species. The grape/wine cluster of strains diverged from the Old World group approximately 1900 years ago, aligning with the expansion of the Roman Empire, and the spread of Vitis vinifera, or the common grape, alongside. The bioprocesses group diverged much earlier, an estimated four millennia ago (around the Neolithic era), showing that yeast was used for food production long before it was domesticated for wine making.
While T. delbrueckii has often been overlooked by winemakers in favor of the more common S. cerevisiae, it has recently been gaining traction for its ability to reduce levels of volatile compounds that negatively affect wine’s flavor and scent. It has also been shown to have a high freezing tolerance when used as a leavening agent, making it of great interest to companies attempting to successfully freeze and transport dough. Though attempts to develop improved strains of this yeast for commercial use have already begun, we previously lacked an understanding of its life-cycle and reproductive habits. In creating this T. delbrueckii family tree, the authors also gained a deeper understanding of the species’ existence, which may help with further development for technological use.
Yeast has weaseled its way into our hearts via our stomachs, and it seems that, in return, we have fully worked our way into its identity. With a bit of teamwork, and perhaps a splash of genetic tweaking, we can continue this fruitful relationship and pursue new opportunities in Epicureanism. I think we would all drink to that!
Related Links:
The Vineyard Yeast Microbiome, a Mixed Model Microbial Map
Reference: Albertin W, Chasseriaud L, Comte G, Panfili A, Delcamp A, et al. (2014) Winemaking and Bioprocesses Strongly Shaped the Genetic Diversity of the Ubiquitous Yeast Torulaspora delbrueckii. PLoS ONE 9(4): e94246. doi:10.1371/journal.pone.0094246
Image 1: Figure 1 from article
Image 2: Figure 3 from article
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Contextualizing the Hobbits
18,000 years ago, the remote Indonesian island of Flores was home to a population of tiny humans. They stood only about 3.5 feet tall on their large feet, and their skulls housed unusually small brains approximately the size of a grapefruit. The identity of these ‘hobbits’ has been hotly debated for years: Were they modern humans suffering a disease, or a new species, Homo floresiensis?
Biological anthropologist Karen Baab first studied a model of LB1, the only skull recovered from the site, at the American Museum of Natural History in 2005. In a recently published PLOS ONE study, she and other researchers compare this specimen to a range of other modern human and extinct hominin skulls to get closer to settling the identity of Homo floresiensis, or ‘Flores man’.
The origins of ‘Flores man’ have been debated for quite a while now. What are the possible origins that are being discussed, and why the uncertainty?
The primary debate has centered on whether LB1 (and possibly the other individuals found on Flores) represents a new species that descended from an extinct species of the genus Homo or whether it is instead a pathological modern Homo sapiens, i.e the same species as us. If the Flores remains do in fact represent a distinct species, then the next question is whether they descended from Homo erectus, a species that may be our direct ancestor, or an even more primitive species. The latter scenario implies an otherwise undocumented migration out of Africa.
What makes it so hard to settle the argument one way or the other?
One of the difficulties in settling this particular argument is that most studies have focused on one or the other of these ideas and compared the Flores remains to either fossil hominins or to pathological modern humans, each using a different set of features. This makes it challenging to compare the alternative hypotheses side-by-side.
What kind of diseases might have caused modern humans to have features similar to these ‘hobbits’?
The three that have been discussed most prominently (and the three we looked at) are microcephaly, endemic hypothyroidism (“cretinism”) and Laron Syndrome. Microcephaly is not a disease per se, but rather a symptom of many different disorders. It refers to having an abnormally small brain and therefore skull. “Cretins” suffer from a lack of thyroid hormone before and after birth, which leads to stunted growth and possibly a slight decrease in skull size. Laron Syndrome individuals produce growth hormone, but their bodies do not properly recognize it, again leading to stunted growth and other developmental issues.
Only a few specimens of this hominin have been found, and there’s only one known skull, from the specimen named LB1. Are there reasons why these specimens have not been discovered elsewhere?
If Homo floresiensis descended from Homo erectus, then their closest relative lived just “next door” on the nearby island of Java. In this case, the unique features of the Homo floresiensis species probably evolved in the isolated island environment of Flores. If, however, the ancestor was a more primitive species, and Homo floresiensis didn’t branch off from H.erectus, it is possible that they might have migrated earlier than known, and we could still find older sites in mainland Asia containing this ancestral species.
You compared the morphology of the LB1 skull to many hominin ancestors and modern human populations from around the world. What were some of the most striking similarities and differences?
The LB1 skull is very distinct from the typical modern human’s, as it has a lower, more elongated silhouette when viewed from the side, , greater width at the rear of the braincase, and a flatter frontal bone (the bone underlying the forehead) with a more pronounced brow ridge. Interestingly, these are some of the same features that distinguish archaic species like Homo erectus from modern humans.
Specimens of Laron Syndrome and “cretin” skulls from modern Homo sapiens presented large, round, globular braincases, which are very different from the smaller, lower and less rounded braincase of LB1. The microcephalic human skulls present a closer comparison to LB1, but still show clear distinctions from LB1 in much the same way that they differ from species like Homo erectus or Homo habilis.
Overall, the LB1 braincase is most similar in its overall shape to small-brained Homo erectus from Eurasia that are 1.8 million years old.
How does this analysis add to, or change, what we knew about Flores man?
This analysis provides a unique opportunity to evaluate these evolutionary and pathological hypotheses side-by-side based on the same criterion – of cranial shape similarity. The results support a stronger affiliation of LB1 with fossil Homo than with any of the proposed pathologies. This study also offers an improvement over previous assessments of the microcephaly hypothesis by using a more extensive sample that better captures the variability in this disorder.
Do these results conclusively settle the discussion? What other possibilities still exist for the origins of H. floresiensis?
While very little in paleoanthropology is ever “settled,” I do think this study represents an important step forward in terms of putting the pathological hypotheses to rest. The question that remains to be answered definitively is which species of archaic Homo is the most likely ancestor of Homo floresiensis – Homo erectus or an earlier and more primitive species of Homo?
Citation: Baab KL, McNulty KP, Harvati K (2013) Homo floresiensis Contextualized: A Geometric Morphometric Comparative Analysis of Fossil and Pathological Human Samples. PLoS ONE 8(7): e69119. doi:10.1371/journal.pone.0069119
Images: Homo floresiensis by Ryan Somma, Cave where the remains of Homo Floresiensis where discovered in 2003, Liang Bua, Flores, Indonesia by Rosino
Hairy, Sticky Leg Pads are In: How Different Spiders Hunt
Spiders are everywhere (Arachnophobes, stop reading now). They’re among the most successful predators on earth today and colonize nearly every terrestrial habitat (that is, not just ceiling corners and under beds), and occasionally do so in numbers large enough to take over small islands. Spider silk may be strong enough to stop a speeding train and some webs, ten times stronger than Kevlar, can be large enough to cross rivers in tropical rainforests.
But more than half of today’s spider species don’t rely on webs or silk to capture their prey. Instead, these hunting spiders have evolved hairy adhesive pads on their legs to grab and hold struggling prey down, according to the results of a recently published PLOS ONE study. The adhesive pads, called scopulae, were commonly seen in many spider species but what wasn’t clear until now was whether they were found in all species, or more likely to occur in hunting spiders.
In this study, researchers used a phylogenetic analysis of spider family trees to correlate different species’ prey capture strategies with the presence or absence of adhesive pads on their legs. They found that the majority of spiders were either web builders or free-ranging hunters, and the latter were most often found to have adhesive hairs on their legs (Apart from these two, at least one rare variety may be mostly vegetarian). Nearly 83% of hunting spiders had adhesive bristles on their legs (compared with 1.1% of web-building varieties). Most of these hunters had either not developed silk-dependent strategies to capture prey, or abandoned web-building for hunting.
Why would so many spiders abandon an obviously successful way to catch prey? Web-building is a useful way to trap insects and some small mammals, but even to a spider, silk is expensive. Creating a web requires work, damages caused by prey or people need frequent repairs, and certain kinds of webs can require large amounts of silk to be effective. The classic orb-web (seen in the picture here) radically reduced these costs, which may be why the spiders that make these are particularly common. However, this new study reveals that hunting has proved at least as successful a strategy as web-building to more than half of today’s spiders.
Bristly scopulae on hunting spiders’ legs have played a big part in this, enabling spiders to grasp and hold on to struggling prey. The thin bristles on scopulae come in many shapes and forms, and also contribute to these spiders’ mad climbing skills. Read more about which spiders evolved these bristles or learn about other arachnid research published in PLOS ONE here.
Citations: Gregori? M, Agnarsson I, Blackledge TA, Kuntner M (2011) How Did the Spider Cross the River? Behavioral Adaptations for River-Bridging Webs in Caerostris darwini (Araneae: Araneidae). PLoS ONE 6(10): e26847. doi:10.1371/journal.pone.0026847
Rogers H, Hille Ris Lambers J, Miller R, Tewksbury JJ (2012) ‘Natural experiment’ Demonstrates Top-Down Control of Spiders by Birds on a Landscape Level. PLoS ONE 7(9): e43446. doi:10.1371/journal.pone.0043446
Wolff JO, Nentwig W, Gorb SN (2013) The Great Silk Alternative: Multiple Co-Evolution of Web Loss and Sticky Hairs in Spiders. PLoS ONE 8(5): e62682. doi:10.1371/journal.pone.0062682
Nyffeler M, Knörnschild M (2013) Bat Predation by Spiders. PLoS ONE 8(3): e58120. doi:10.1371/journal.pone.0058120
Images: Foot of the little jumping spider Euophrys frontalis, credit Jonas Wolff; varied shapes and sizes of bristles on scopulae from pone.0062682; spider web on plant by mikebaird