David M. Wilkinson

Is There a Size Limit for Cosmopolitan Distribution in Free-Living Microorganisms? A Biogeographical Analysis of Testate Amoebae from Polar Areas

A long-standing debate in microbial ecology is the extent to which free-living microorganisms exhibit cosmopolitan distributions. We use a comparison of testate amoebae communities in cold “polar” locations (Arctic, Antarctic, and Tibet) to investigate how a microorganism’s size affects its probability of having a cosmopolitan distribution. We show that the probability a given taxa being reported in all three locations increases as testate size decreases. Likewise, excluding those testates found only in Tibet, very small testates (<20xa0μm) are more likely to occur in both the Arctic and Antarctic than in either of these poles alone. Attempting to correct for phylogeny reduces the number of statistically significant relationships—both because of decreased sample size and potentially real phylogenetic patterns, although some size-dependent effects were still apparent. In particular, taxa found in both the Arctic and Antarctic poles were significantly smaller than congeneric taxa found only in Tibet. This pattern may in part be due to habitat effects, with the Tibetan samples being more likely to have come from aquatic sites which may be more suitable for larger taxa. Overall, our analysis suggests that, at least within testate amoebae, a cosmopolitan distribution becomes increasingly common as median taxon size decreases.

Phytoplankton Communities Exhibit a Stronger Response to Environmental Changes than Bacterioplankton in Three Subtropical Reservoirs

The simultaneous analysis of multiple components of ecosystems is crucial for comprehensive studies of environmental changes in aquatic ecosystems, but such studies are rare. In this study, we analyzed simultaneously the bacterioplankton and phytoplankton communities in three Chinese subtropical reservoirs and compared the response of these two components to seasonal environmental changes. Time-lag analysis indicated that the temporal community dynamics of both bacterioplankton and phytoplankton showed significant directional changes, and variance partitioning suggested that the major reason was the gradual improvement of reservoir water quality from middle eutrophic to oligo-mesotrophic levels during the course of our study. In addition, we found a higher level of temporal stability or stochasticity in the bacterioplankton community than in the phytoplankton community. Potential explanations are that traits associated with bacteria, such as high abundance, widespread dispersal, potential for rapid growth rates, and rapid evolutionary adaptation, may underlie the different stability or stochasticity of bacterioplankton and phytoplankton communities to the environmental changes. In addition, the indirect response of bacterioplankton to nitrogen and phosphorus may result in the fact that environmental deterministic selection was stronger for the phytoplankton than for the bacterioplankton communities.

DNA metabarcoding reveals that 200 μm size‐fractionated filtering is unable to discriminate between planktonic microbial and large eukaryotes

Microeukaryotic plankton (0.2–200 μm) are critical components of aquatic ecosystems and key players in global ecological processes. High‐throughput sequencing is currently revolutionizing their study on an unprecedented scale. However, it is currently unclear whether we can accurately, effectively and quantitatively depict the microeukaryotic plankton communities using traditional size‐fractionated filtering combined with molecular methods. To address this, we analysed the eukaryotic plankton communities both with, and without, prefiltering with a 200 μm pore‐size sieve –by using SSU rDNA‐based high‐throughput sequencing on 16 samples with three replicates in each sample from two subtropical reservoirs sampled from January to October in 2013. We found that ~25% reads were classified as metazoan in both size groups. The species richness, alpha and beta diversity of plankton community and relative abundance of reads in 99.2% eukaryotic OTUs showed no significant changes after prefiltering with a 200 μm pore‐size sieve. We further found that both >0.2 μm and 0.2–200 μm eukaryotic plankton communities, especially the abundant plankton subcommunities, exhibited very similar, and synchronous, spatiotemporal patterns and processes associated with almost identical environmental drivers. The lack of an effect on community structure from prefiltering suggests that environmental DNA from larger metazoa is introduced into the smaller size class. Therefore, size‐fractionated filtering with 200 μm is insufficient to discriminate between the eukaryotic plankton size groups in metabarcoding approaches. Our results also highlight the importance of sequencing depth, and strict quality filtering of reads, when designing studies to characterize microeukaryotic plankton communities.

Multiple states of environmental regulation in well-mixed model biospheres

The Gaia hypothesis postulates that life influences Earths feedback mechanisms to form a self regulating system. This provokes the question: how can global self-regulation evolve? Most models demonstrating environmental regulation involving life have relied on alignment between local selection and global regulation. In these models environment-improving individuals or communities spread to outcompete environment degrading individuals/communities, leading to global regulation, but this depends on local differences in environmental conditions. In contrast, well-mixed components of the Earth system, such as the atmosphere, lack local environmental differentiation. These previous models do not explain how global regulation can emerge in a system with no well defined local environment, or where the local environment is overwhelmed by global effects. We present a model of self-regulation by microbes in an environment with no spatial structure. These microbes affect an abiotic temperature as a byproduct of metabolism. We demonstrate that global self-regulation can arise in the absence of spatial structure in a diverse ecosystem without localised environmental effects. We find that systems can exhibit nutrient limitation and two temperature limitation regimes where the temperature is maintained at a near constant value. During temperature regulation, the total temperature change caused by the microbes is kept near constant by the total population expanding or contracting to absorb the impacts of new mutants on the average affect on the temperature per microbe. Dramatic shifts between low temperature regulation and high temperature regulation can occur when a mutant arises that causes the sign of the temperature effect to change. This result implies that self-regulating feedback loops can arise without the need for spatial structure, weakening criticisms of the Gaia hypothesis that state that with just one Earth, global regulation has no mechanism for developing because natural selection requires selection between multiple entities.

Selection for Gaia across Multiple Scales

Recently postulated mechanisms and models can help explain the enduring Gaia puzzle of environmental regulation mediated by life. Natural selection can produce nutrient recycling at local scales and regulation of heterogeneous environmental variables at ecosystem scales. However, global-scale environmental regulation involves a temporal and spatial decoupling of effects from actors that makes conventional evolutionary explanations problematic. Instead, global regulation can emerge by a process of sequential selection in which systems that destabilize their environment are short-lived and result in extinctions and reorganizations until a stable attractor is found. Such persistence-enhancing properties can in turn increase the likelihood of acquiring further persistence-enhancing properties through selection by survival alone. Thus, Earth system feedbacks provide a filter for persistent combinations of macroevolutionary innovations.

Gaian bottlenecks and planetary habitability maintained by evolving model biospheres: The ExoGaia model

The search for habitable exoplanets inspires the question - how do habitable planets form? Planet habitability models traditionally focus on abiotic processes and neglect a biotic response to changing conditions on an inhabited planet. The Gaia hypothesis postulates that life influences the Earths feedback mechanisms to form a self-regulating system, and hence that life can maintain habitable conditions on its host planet. If life has a strong influence, it will have a role in determining a planets habitability over time. We present the ExoGaia model - a model of simple planets host to evolving microbial biospheres. Microbes interact with their host planet via consumption and excretion of atmospheric chemicals. Model planets orbit a star which provides incoming radiation, and atmospheric chemicals have either an albedo, or a heat-trapping property. Planetary temperatures can therefore be altered by microbes via their metabolisms. We seed multiple model planets with life while their atmospheres are still forming and find that the microbial biospheres are, under suitable conditions, generally able to prevent the host planets from reaching inhospitable temperatures, as would happen on a lifeless planet. We find that the underlying geochemistry plays a strong role in determining long-term habitability prospects of a planet. We find five distinct classes of model planets, including clear examples of Gaian bottlenecks - a phenomenon whereby life either rapidly goes extinct leaving an inhospitable planet, or survives indefinitely maintaining planetary habitability. These results suggest that life might play a crucial role in determining the long-term habitability of planets.

Taxonomic Implications of Morphological Complexity Within the Testate Amoeba Genus Corythion from the Antarctic Peninsula

Precise and sufficiently detailed morphological taxonomy is vital in biology, for example in the accurate interpretation of ecological and palaeoecological datasets, especially in polar regions, where biodiversity is poor. Testate amoebae on the Antarctic Peninsula (AP) are well-documented and variations in their population size have recently been interpreted as a proxy for microbial productivity changes in response to recent regional climate change. AP testate amoeba assemblages are dominated by a small number of globally ubiquitous taxa. We examine morphological variation in Corythion spp. across the AP, finding clear evidence supporting the presence of two morphospecies. Corythion constricta (Certes 1889) was identified on the AP for the first time and has potentially been previously misidentified. Furthermore, a southerly trend of decreasing average test size in Corythion dubium (Taránek 1881) along the AP suggests adaptive polymorphism, although the precise drivers of this remain unclear, with analysis hindered by limited environmental data. Further work into morphological variation in Corythion is needed elsewhere, alongside molecular analyses, to evaluate the potential for (pseudo)cryptic diversity within the genus. We advocate a parsimonious taxonomical approach that recognises genetic diversity but also examines and develops accurate morphological divisions and descriptions suitable for light microscopy-based ecological and palaeoecological studies.

Large-scale biogeographical patterns of bacterial antibiotic resistome in the waterbodies of China

Antibiotic resistance genes (ARGs) are widespread in aquatic environments, but we know little about their biogeographical distribution and occurrence at national scales. Here we analyzed the patterns of ARGs from 42 natural waterbodies (natural lakes and reservoirs) across China using high-throughput approaches. The major ARGs were multidrug genes and the main resistance mechanism was the efflux pump. Although the absolute abundance of ARGs (gene copies/L) in the south/central waterbodies was similar to the northern waterbodies, the normalized abundance of ARGs (ARGs/16S rRNA gene copy number) was higher in the south/central waterbodies than in the north (mainly because of the aminoglycoside and multidrug resistance genes). Human activities strongly correlated with the normalized abundance of ARGs. The composition of ARGs in the waterbodies of south/central China was different from that in the north, and ARGs showed a distance-decay relationship. Anthropogenic factors had the most significant effects on this spatial distribution of ARG composition, followed by the spatial, bacterial and physicochemical factors. These indicate that the ARGs exhibited biogeographical patterns and that multiple ecological mechanisms - such as environmental selection (human activities and local physicochemical parameters) and dispersal limitation - influence distribution of ARGs in these waters. In general, our results provide a valuable ecological insight to explain the large-scale dispersal patterns in ARGs, thereby having potential applications for both public health and environmental management.

Alternative Mechanisms for Gaia

A long-standing objection to the Gaia hypothesis has been a perceived lack of plausible mechanisms by which life on Earth could come to regulate its abiotic environment. A null hypothesis is survival by pure chance, by which any appearance of regulation on Earth is illusory and the persistence of life simply reflects the weak anthropic principle - it must have occurred for intelligent observers to ask the question. Recent work has proposed that persistence alone increases the chance that a biosphere will acquire further persistence-enhancing properties. Here we use a simple quantitative model to show that such selection by survival alone can indeed increase the probability that a biosphere will persist in the future, relative to a baseline of pure chance. Adding environmental feedback to this model shows either an increased or decreased survival probability depending on the initial conditions. Feedback can hinder early life becoming established if initial conditions are poor, but feedback can also prevent systems from diverging too far from optimum environmental conditions and thus increase survival rates. The outstanding question remains the relative importance of each mechanism for the historical and continued persistence of life on Earth.