It is with great pleasure that we announce the launch of our Biodiversity Conservation Collection. This Collection showcases research on a broad range of conservation science related topics, including anthropogenic impacts on biodiversity, such
It is with great pleasure that we announce the launch of our Biodiversity Conservation Collection. This Collection showcases research on a broad range of conservation science related topics, including anthropogenic impacts on biodiversity, such as habitat degradation, the spread of invasive species and global warming; conservation of key ecosystem services, such as carbon sequestration and pest regulation; and new management strategies to prevent further biodiversity loss.
We are extremely grateful to our team of Guest Editors, Steve Beissinger (University of California, Berkeley), Thomas Couvreur (Pontificia Universidad Catolica del Ecuador), Carlos Duarte (KAUST), Claudia Mettke-Hoffmann (Liverpool John Moores University) and Stuart Pimm (Duke University), for evaluating all submitted research and selecting articles for inclusion in the Collection. We also want to express our thanks to the PLOS ONE Academic Editors involved in the handling of submissions, to the reviewers, and to all the authors who submitted their research to this Call for Papers.
Eight of the studies published in the initial Collection release focus on habitat destruction in a wide range of regions, ecosystems and species. In the North Pacific Ocean, Edwards et al. investigated the ecological consequences of marine deforestation caused by shifting trophic interactions in the Aleutian Archipelago. They show that the rapid decline of sea otter populations, caused by increased predation pressure from killer whales, led to high sea urchin densities causing widespread deforestation of the kelp forests and general loss of biodiversity and ecosystem function. In the mainland USA, Bradshaw et al. evaluated whether wetland management practices for waterfowl were also beneficial to other wetland-dependent species such as bitterns, grebes and crakes. Habitats for marsh bird species have more than halved in the last 50 years due to wetland loss and degradation; their results highlight the importance of maintaining wetland hydrologic and vegetation complexity for the conservation of breeding marsh birds.
In Brazil, three independent studies provide evidence of the impacts of habitat fragmentation in the Amazon rain forest, where biodiversity has rapidly declined in recent decades. Palmeirim et al. quantified the effect of deforestation on small mammals and found that forest dwelling species are being replaced by open-habitat species as the deforestation frontier expands. Teixeira-Santos et al. studied four endangered emblematic large terrestrial mammals and showed that the survival ability was different for each species and that some species can adapt to tolerate anthropogenically altered habitats. Paschoalini et al. studied the effects of habitat fragmentation on the Araguaian river dolphin, whose populations have been dramatically reduced due to dam construction. This research provides potential practical applications to help species management and conservation in the region, as occupation and development of the Amazon is currently being encouraged in Brazil.
When the habitat is fragmented, isolated populations lose genetic diversity, leaving them more vulnerable to changing environmental conditions and with a higher risk of extinction. In the Midwestern USA, Douglas et al. examined the genetic population structure of three upland game birds inhabiting the declining American prairie grasslands, including the endangered Greater Prairie Chicken, and found that their populations are experiencing a genetic bottleneck. They advocate for a multi-species approach as a more effective management strategy for endangered upland game birds and for making more land available to prairie species. In the United Kingdom, Ball et al. conducted a study on the conservation genetic state of adder populations and found that the species’ polyandrous breeding system is, for the moment, protecting it against inbreeding. However, this might become a problem in the future as loss of connectivity prevents movement of individuals between patches of suitable habitat. Dondina et al. studied the suitability of ecological corridors to connect two isolated wolf populations through the degraded lowlands of Northern Italy and showed the importance of keeping natural areas, such as rivers, for maintaining habitat connectivity for the conservation of endangered species in a fragmented landscape.
Three studies among the first batch of articles published in this Collection address the impacts of climate change on biodiversity and potential mitigation strategies. Carbon sequestration has been suggested as a potential approach to mitigating the effects of greenhouse gas emissions responsible for global warming. In Spain, Morant et al. investigated the relationships between wetlands’ ecological characteristics, conservation measures and carbon emissions in the Ebro Delta wetlands. Wetlands are an important ecosystem service acting as natural carbon sinks but are under threat due to habitat destruction.
Large-scale empirical studies of the existing and projected impacts of climate change on wildlife are vital to scientifically-informed conservation management strategies aimed at minimizing and mitigating these impacts. In Southern California, Fogarty et al. used a large bird abundance dataset to investigate whether annual variation in seasonal temperature and precipitation was associated with relative abundances of breeding bird species. They found that species in arid areas may be negatively affected by increased temperature and aridity, but species from cooler areas may respond positively to those fluctuations in climate. Carbon pricing policies can also have unintended consequences for biodiversity through changing land management. Hashida et al. modelled forest habitat changes in response to forest landowner decision-making under multiple carbon pricing scenarios in Western USA. Their results predict a major shift from coniferous forest to hardwoods which could result in a dramatic loss of biodiversity in the region.
Three studies published in the Collection showcase research on species invasions. International trade is a major pathway of introduction of invasive species. Lucardi et al. conducted a comprehensive survey of the plant community at the largest container terminal in the USA . Their research identified the presence of a high number of invasive plant species in the port, providing important evidence that shipping ports are crucial sources of emergent plant invasions but are largely under-researched. Invasive species can have complex ecological impacts on the regions of invasion. Besterman et al. studied the ecological impacts of the establishment of one of the most invasive macroalgae on habitat selection and foraging behaviour of shorebirds in the mid-Atlantic region of the USA and found that generalist species preferred invaded habitats while specialist shorebirds preferred uninvaded mudflats. Invasive species also cause major economic losses in the regions of invasion. One of the most successful methods for sustainable management of invasive species is using their own natural enemies against them. In Morocco, Qessaoui et al. discovered the insecticidal activity of native rhizobacteria present in the soil against an important pest of tomato crops and suggested that using biological control agents would reduce the amount of synthetic chemical pesticides being used to control plant pests.
Finally three papers report methodological advances in conservation of endangered species. Endangered species are usually difficult to study because their population densities are low which hampers conservation efforts. Here, Nagarajan et al. report successful results of a non-invasive method for monitoring a wood-boring beetle species threatened by habitat loss in California. Current monitoring efforts require extensive field work looking for this rare species. In this study, the authors collected faecal samples from exit holes on trees and applied genetic barcoding techniques to identify the makers of the holes.
Large terrestrial carnivores are often keystone species in the ecosystems but have historically been persecuted and their populations are in decline globally. In the USA, sport hunting is used as a tool for managing puma populations. Laundré et al. investigated the effectiveness of this strategy for reducing conflict with humans, livestock and game species. Their results indicate that there is little evidence that puma control reduces conflict, and remark the need to reassess traditional predator control practices.
Management of captive populations is crucial for conservation of endangered species whose wild populations are at high risk of extinction. Fazio et al. studied the stress physiology of the fishing cat, a threatened wild cat from Southeast Asia, that is notoriously difficult to breed in captivity. Their study suggests that management actions such as transfers between facilities increases levels of stress while reduced animal-keeper interaction and social housing could lower stress levels and increase breeding success. This study might provide insights to better manage translocations of captive individuals of easily stressed species.
At the time of launch, there are 17 research articles featured in the Collection but more papers will be added as they are published over the coming weeks – so do check back for updates!
About the Guest Editors:
Steve Beissinger is Professor of Ecology & Conservation Biology at the University of California, Berkeley, where he held the A. Starker Leopold Chair in Wildlife Biology (2003-13), is a research associate of the Museum of Vertebrate Zoology, and is the co-Director of the Berkeley Institute for Parks, People and Biodiversity. Professor Beissinger’s current research centers on wildlife responses to global change and species’ extinctions – with recent fieldwork carried out in protected areas and working landscapes in California and Latin America. He directs the Grinnell Resurvey Project – a 15 year effort to revisit locations throughout California first surveyed by Joseph Grinnell in the early 1900’s in order to quantify the impacts of a century of climate and land-use change on the birds and mammals of California. Steve’s studies of parrotlets in Venezuela extend more than 30 years. Integrative studies of secretive, threatened rails in California provide a model for understanding coupled natural and human systems. He has authored over 200 scientific publications and is senior editor of three books. He served on the editorial boards of Ecology Letters, Ecology, Conservation Biology, Studies in Avian Biology, and Climate Change Responses. Steve is a Fellow of the American Association for the Advancement of Science, the Ecological Society of America (ESA), the Wissenschaftskolleg zu Berlin, and the American Ornithological Society, which awarded him the William Brewster Memorial Award in 2010 for his research on Western Hemisphere birds.
Thomas L.P. Couvreur is a senior researcher at the French National Institute for Sustainable Development, and is currently based at the “Pontificia Universidad Catolica del Ecuador”, in Quito Ecuador. He received his PhD in tropical biodiversity from the Wageningen University in the Netherlands, and worked as post doc at the Osnabruck University in Germany and The New York Botanical Garden in the USA. His main interest lies in understanding the evolution, resilience and diversity of tropical biodiversity, and rain forests in particular, one of the most complex and diverse ecosystems on the planet. He undertakes research in taxonomy, conservation, molecular phylogenetics and phylogeography of tropical plants. His research mainly focuses on tropical Africa and South America. He is chair of the IUCN Species Survival Commission for palms since 2018.
Professor Carlos M. Duarte (Ph.D. McGill University, 1987) is the Tarek Ahmed Juffali Research Chair in Red Sea Ecology at the King Abdullah University of Science and Technology (KAUST), in Saudi Arabia. Before this he was Research Professor with the Spanish National Research Council (CSIC) and Director of the Oceans Institute at The University of Western Australia.
Duarte’s research focuses on understanding the effects of global change in aquatic ecosystems, both marine and freshwater. He has conducted research across all continents and oceans, spanning most of the marine ecosystem types, from inland to near-shore and the deep sea and from microbes to whales. Professor Duarte led the Malaspina 2010 Expedition that sailed the world’s oceans to examine the impacts of global change on ocean ecosystems and explore their biodiversity. Professor Duarte served as President of the American Society of Limnology and Oceanography between 2007 and 2010. In 2009, was appointed member of the Scientific Council of the European Research Council (ERC), the highest-level scientific committee at the European Level, where he served until 2013. He has published more than 700 scientific papers and has been ranked within the top 1% Highly-Cited Scientist by Thompson Reuters in all three assessments of this rank, including the 2018 assessment released by Clarivate Analytics.
Dr Claudia Mettke-Hofmann is Reader in Animal Behaviour at Liverpool John Moores University, UK, and Subject Leader of the Animal Behaviour team. She received her externally conducted PhD from Free University of Berlin, Germany, and subsequently worked as a postdoc at the Max-Planck Institute for Ornithology in Radolfzell and Andechs, Germany, in collaboration with the Konrad Lorenz Institute for Comparative Behaviour, Vienna, Austria, before moving to the Smithsonian Migratory Bird Center, Washington DC, USA. She is now based at Liverpool John Moores University. Her research area is cognitive ecology, mainly in birds, with strong links to conservation aspects and animal welfare. She investigates how animals collect and store environmental information in relation to their ecology on the species level but also on the individual level (personality). A focus is how animals respond to environmental change, particularly in species that differ in their movement patterns such as being resident, migratory or nomadic. Differences in cognitive abilities in these groups help explain and predict population developments in our rapidly changing environments. More recently, her research has focussed on individual differences in cognition in colour-polymorphic species highlighting exciting differences in responses to environmental change between colour morphs. Claudia has been a PLOS ONE Section Editor since 2014.
Stuart Pimm is the Doris Duke Chair of Conservation Ecology at the Nicholas School of the Environment at Duke University. He is a world leader in the study of present day extinctions and what we can do to prevent them. Pimm received his BSc degree from Oxford University in 1971 and his Ph.D from New Mexico State University in 1974. Pimm is the author of over 300 scientific papers and four books. Pimm directs SavingSpecies, a 501c3 non-profit that uses funds for carbon emissions offsets to fund local conservation groups to restore degraded lands in areas of exceptional tropical biodiversity. His international honours include the Tyler Prize for Environmental Achievement (2010), the Dr. A.H. Heineken Prize for Environmental Sciences from the Royal Netherlands Academy of Arts and Sciences (2006).
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PLOS ONE is organizing a Twitter chat on citizen science methodologies on 2nd April- see details below
Citizen science (CS) encompasses a broad range of research methodologies that involve public participation for data collection, transcription or analysis. Applications of CS have been found in many disciplines, but ecology has consistently been at the forefront. While some CS-based ecological monitoring schemes- such as the UK Butterfly Monitoring Scheme, established in 1976- have been running for decades, the popularity of CS has grown rapidly in more recent years. A wide range of projects based on CS methodologies are now being undertaken around the world, at local, national and international scales. The value of volunteer participation in activities ranging from transect-based species monitoring (Wepprich et al., 2019) and collection of biological specimens for lab-based analysis (Larson et al., 2020; Rasmussen et al., 2020) to crowdsourcing of creative thinking for study design (Can et al., 2017), has been repeatedly demonstrated. Studies have also highlighted the particular utility of CS methodologies in supporting long-term ecological monitoring in resource-limited contexts, including in economically developing countries (Gouraguine et al., 2019). Meanwhile, examples of the real-world impact of CS research are abundant, both in specific ecological interventions and the wider political discourse. For instance, the influential UK State of Nature 2019 report, likely to be a key source of evidence for future environmental legislation, cites the outcomes of a wealth of CS projects.
With the expansion of CS research, there is lively debate about how to maximise rigor and reproducibility in different types of CS methodologies. One of the crucial aspects of a successful CS study is an appropriately designed protocol, which features a realistic degree of complexity and accounts for the specific challenges of handling CS-derived data. An example of this is provided by a recent comprehensive report of the design, launch and assessment of the UK National Plant Monitoring Scheme (Pescott et al., 2019). Pre-testing of protocols prior to project launch can provide confidence in the robustness of the study design. When designing a CS study, it is also important to understand volunteer motivation and ensure that this is appropriately matched with the nature of the task to be performed (Lyons & Zhang, 2019). Some CS studies utilize narrower demographic groups to meet the required level of motivation and understanding, such as amateur naturalists (Hallmann et al., 2017) or students who are following a course in a related topic (Chiovitti et al., 2019). Depending on the type of study, researchers may also plan to support CS volunteers with training or technological aids, increasingly in the form of mobile apps (Ožana et al., 2019; Appenfeller et al., 2020).
A certain amount of error, either random or systematic, is likely to be introduced by the collection of data by CS volunteers, and study designs must account for this. The level of error can be reduced by allowing volunteers to provide clarifying metadata or to register uncertainty (Torre et al., 2019), or using incentives to reduce sampling bias (Callaghan et al., 2019), but researchers should also ensure that they have means to assess the accuracy of contributed data (Falk et al., 2019; Gibson et al., 2019). Much ecological research is based on large public databases of volunteer-contributed records of species distributions, phenological events and other observational data (e.g. Siljamo et al., 2020). There is an active discussion in the ecological research community about how to maximize the reliability and utility of such data (Ball-Damerow et al., 2019).
The particular considerations that have to be made in the design, execution and evaluation of CS studies has led to calls for dedicated standards and guidelines for CS research. Of course, any such tools must strike the balance between promoting appropriate levels of standardization and allowing the flexibility required for applications of CS methodologies across diverse settings and research questions. Whilst some progress has been made towards this goal, maintaining an open and constructive dialogue among CS practitioners and other stakeholders remains critical to ensure that researchers, volunteers and society are able to realize the full potential of CS.
To foster discussion of these important issues, PLOS ONE (@plosone) will be moderating a Twitter chat on citizen science methodologies on Thursday 2nd April starting at 4pm BST (8am PDT, 11am EDT, 5pm CET). This is a chance for the CS community to share perspectives, experiences and suggestions for best practice. We’ll aim to cover the following questions (and more!):
- How far can methods in CS projects be standardized?
- What steps should be taken to maximize CS data quality?
- Is there a need for clearer guidelines for the design and execution of CS studies?
- How should credit for data collection be apportioned?
You can take part by using the hashtag #citscichat– we hope to see you there!
Appenfeller LR, Lloyd S, Szendrei Z (2020) Citizen science improves our understanding of the impact of soil management on wild pollinator abundance in agroecosystems. PLoS ONE 15(3): e0230007. https://doi.org/10.1371/journal.pone.0230007
Ball-Damerow JE, Brenskelle L, Barve N, Soltis PS, Sierwald P, Bieler R, et al. (2019) Research applications of primary biodiversity databases in the digital age. PLoS ONE 14(9): e0215794. https://doi.org/10.1371/journal.pone.0215794
Callaghan CT, Rowley JJL, Cornwell WK, Poore AGB, Major RE (2019) Improving big citizen science data: Moving beyond haphazard sampling. PLoS Biol 17(6): e3000357. https://doi.org/10.1371/journal.pbio.3000357
Can ÖE, D’Cruze N, Balaskas M, Macdonald DW (2017) Scientific crowdsourcing in wildlife research and conservation: Tigers (Panthera tigris) as a case study. PLoS Biol 15(3): e2001001. https://doi.org/10.1371/journal.pbio.2001001
Chiovitti A, Thorpe F, Gorman C, Cuxson JL, Robevska G, Szwed C, et al. (2019) A citizen science model for implementing statewide educational DNA barcoding. PLoS ONE 14(1): e0208604. https://doi.org/10.1371/journal.pone.0208604
Falk S, Foster G, Comont R, Conroy J, Bostock H, Salisbury A, et al. (2019) Evaluating the ability of citizen scientists to identify bumblebee (Bombus) species. PLoS ONE 14(6): e0218614. https://doi.org/10.1371/journal.pone.0218614
Gibson KJ, Streich MK, Topping TS, Stunz GW (2019) Utility of citizen science data: A case study in land-based shark fishing. PLoS ONE 14(12): e0226782. https://doi.org/10.1371/journal.pone.0226782
Gouraguine A, Moranta J, Ruiz-Frau A, Hinz H, Reñones O, Ferse SCA, et al. (2019) Citizen science in data and resource-limited areas: A tool to detect long-term ecosystem changes. PLoS ONE 14(1): e0210007. https://doi.org/10.1371/journal.pone.0210007
Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N, Schwan H, et al. (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12(10): e0185809. https://doi.org/10.1371/journal.pone.0185809
Larson RN, Brown JL, Karels T, Riley SPD (2020) Effects of urbanization on resource use and individual specialization in coyotes (Canis latrans) in southern California. PLoS ONE 15(2): e0228881. https://doi.org/10.1371/journal.pone.0228881
Lyons E, Zhang L (2019) Trade-offs in motivating volunteer effort: Experimental evidence on voluntary contributions to science. PLoS ONE 14(11): e0224946. https://doi.org/10.1371/journal.pone.0224946
Ožana S, Burda M, Hykel M, Malina M, Prášek M, Bárta D, et al. (2019) Dragonfly Hunter CZ: Mobile application for biological species recognition in citizen science. PLoS ONE 14(1): e0210370. https://doi.org/10.1371/journal.pone.0210370
Pescott OL, Walker KJ, Harris F, New H, Cheffings CM, Newton N, et al. (2019) The design, launch and assessment of a new volunteer-based plant monitoring scheme for the United Kingdom. PLoS ONE 14(4): e0215891. https://doi.org/10.1371/journal.pone.0215891
Rasmussen SL, Nielsen JL, Jones OR, Berg TB, Pertoldi C (2020) Genetic structure of the European hedgehog (Erinaceus europaeus) in Denmark. PLoS ONE 15(1): e0227205. https://doi.org/10.1371/journal.pone.0227205
Siljamo P, Ashbrook K, Comont RF, Skjøth CA (2020) Do atmospheric events explain the arrival of an invasive ladybird (Harmonia axyridis) in the UK? PLoS ONE 15(1): e0219335. https://doi.org/10.1371/journal.pone.0219335
Torre M, Nakayama S, Tolbert TJ, Porfiri M (2019) Producing knowledge by admitting ignorance: Enhancing data quality through an “I don’t know” option in citizen science. PLoS ONE 14(2): e0211907. https://doi.org/10.1371/journal.pone.0211907
Wepprich T, Adrion JR, Ries L, Wiedmann J, Haddad NM (2019) Butterfly abundance declines over 20 years of systematic monitoring in Ohio, USA. PLoS ONE 14(7): e0216270. https://doi.org/10.1371/journal.pone.0216270
All images used under Pixabay licence.
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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 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.
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.
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 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.
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.
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.
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 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 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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PLOS ONE has an open Call for Papers on the Microbial Ecology of Changing Environments, with selected submissions to be featured in an upcoming Collection. We aim to highlight a range of interdisciplinary articles showcasing the diversity of systems, scales, interactions and applications in this dynamic field of research.
What makes microbes so interesting?
MC: Microorganisms are everywhere and are important members of all of the ecosystems they inhabit. There are microorganisms in soils, oceans, lakes, and even within our bodies. Within all of these habitats they are performing really important functions. In lakes, oceans, and soils, microorganisms are key to moving nutrients around. Within our bodies, they aid in things like digestion and disease prevention.
SK: Microorganisms are fascinating in how genetically diverse and numerous they are. Microorganisms can be found in almost every habitat on Earth and are often the first to respond to environmental disturbance and global change. Thus, microorganisms likely hold the key to solving most of Earth’s problems as we face global climate change.
How is microbial ecology relevant to major environmental and societal issues like climate change and food security?
MC: Given how ubiquitous microorganisms are across the world, understanding how they function is key if we want to understand and mitigate the consequences of climatic change and if we want to grow food more sustainably and in marginal lands. For instance, if we can get a better understanding of microbial carbon cycling, we can potentially use biological carbon capture as a mitigation strategy to help combat rising levels of atmospheric carbon dioxide. Additionally, researchers around the world are trying to understand how plants interact with microbial communities in an effort to harness these microbes to increase food production and the ability of plants to withstand changing abiotic conditions.
SK: Microorganisms are the key for innovating nature-based solutions to climate change. For example, specific fungal symbionts of plants can be tailored to increase agricultural plant drought tolerance. Other microorganisms may be deployed to remediate oil spills or other man-made pollutants. Finally, engineering plant-microbial associations may lead to a larger terrestrial carbon sink to offset atmospheric CO2 concentrations, creating a negative feedback to climate change itself.
Tell us a bit about your own research and how it ties in with some of these issues.
MC: A large portion of my research is focused on understanding how to use beneficial microbes to increase plant productivity and tolerance to drought, and also in understanding how these communities function in the soil environment with the ultimate goal of using them to enhance ecosystem stability. I am part of two large multi-disciplinary teams at Oak Ridge National Laboratory that are specifically focused on plant-microbe interactions in the potential biofuel feedstock, Populus. We are trying to characterize basic principles governing plant-microbe interactions in the hope of making Populus a better biofuel that can grow in marginal lands with limited input of fertilizer and water.
SK: Research in the Kivlin Lab aims to create distribution models for terrestrial microorganisms and their functions. Our current focus is on arbuscular mycorrhizal (AM) fungi, as these plant symbionts are the main providers of nutrients and drought tolerance to agricultural plants. We are interested in where these fungi are, the ecosystem-level carbon and nutrient cycling they promote and how sensitive these plant-fungal interactions may be to climate change. To address these questions, we both compile data on AM fungal distributions worldwide, but also examine plant-AM fungal interactions along altitudinal gradients that serve as a space for time substitution for climate change and in long-term climate change experiments.
How are technological advances opening up new opportunities in your field?
MC: Over the last 20 years there have been rapid advances in sequencing and molecular techniques that have enabled amazing opportunities in microbial and ecosystem ecology. We are finally able to identify unculturable microorganisms inhabiting diverse communities using next generation sequencing and are getting clues into their function using metagenomics, metatranscriptomics, proteomics, and metabolomics. Further, using these techniques, people are developing some new strategies to culture more microbes.
SK: It is increasingly clear that the genomics revolution has impacted microbial ecology. We now can link functional genetic potential to microorganisms in environmental microbiomes and understand how interactions among microorganisms and between microorganisms and plants control expression of these functional genes and the metabolites they code for.
How does microbial ecology benefit from interdisciplinary collaboration?
MC: Microbial communities are incredibly complex, therefore understanding their role in ecosystems really requires a systems biology approach. Because of this, having an interdisciplinary team to tackle questions at various scales is really important.
SK: Microbial ecology is inherently interdisciplinary. We collaborate with earth system modelers to scale microbial function from the organism to the globe and with geneticists to understand the genetic underpinnings of those functions. Without these collaborations, our field would be siloed to case-studies of microbial communities and lack the ability to develop first-principles theory across microbial communities and environments.
What are some of the biggest unsolved questions in microbial ecology?
MC: There are so many unsolved questions in microbial ecology that it is hard to just identify a few. We still have a limited understanding of how microbial communities fluctuate through time. How stable are they within ecosystems? Are organisms within communities functionally redundant? Does this redundancy aid in resilience of the community post disturbance? How do these communities respond to fluctuations in abiotic variables? I could really go on and on.
SK: Despite all of the vital roles that microorganisms provide in the environment, we still don’t understand (1) where microorganisms even are spatially and what abiotic and biotic processes control these distributions, or (2) how temporally dynamic microbial communities are both within and among plant growing seasons. Answering these fundamental questions will allow us to understand linkages between microbial communities and plant growth, microbial composition and ecosystem carbon and nutrient cycles, and allow us to effectively manipulate microbial consortia for societal gain in agricultural and bioremediation settings.