Implications of invasion biology for resurrected pathogens

Despite current advances in our understanding of biological invasions, little is known about the biology of non‐native pathogens (i.e., disease‐causing pathogens including viruses, bacteria, fungi, protists, and nematodes) and their impact on biodiversity and emergence of zoonotic diseases after introduction into new regions (Hulme, 2014; Roy et al., 2016).

Pathogens are frequent players in biological invasions because they are either introduced into new communities along with invading species or left behind in the ancestral range of the host, affording the host “enemy release” (such enemy release is predicted to enhance competitive ability in the new range, and this is particularly important for competitively dominant species that are limited by pathogens in their original range; Dunn & Hatcher, 2015).

The introduction of non‐native pathogens can lead to new host–pathogen or pathogen–pathogen interactions (Dunn & Hatcher, 2015). The consequences of exposure of non‐native pathogens to the community are difficult to predict (Boissier et al., 2016). To date, attention has largely focused on major diseases of humans, domesticated livestock, and cultivated plants. The spread of non‐native pathogens, which affect wildlife, has received less attention despite the magnitude of their potential effects on endangered species, ecosystems, and ecosystem services (Roy et al., 2016).

Predictions of future risks have focused on how climate change might shift the distribution of hosts and/or vectors, alter the timing of their life cycles, and subsequently facilitate the establishment of new host–pathogen combinations which can lead to atypical disease scenarios (Hulme, 2014). The following are a few examples of non‐native pathogens that have entered a native community and have devastating effects on biodiversity.

The worldwide amphibian decline is driven by environmental change and ecological novelty including habitat loss, hunting, environmental trade, and the emerging infectious disease chytridiomycosis (Crawford, Lips, & Bermingham, 2010; Dunn & Hatcher, 2015). This disease is caused by Batrachochytrium dendrobatidis, an invasive fungus infecting over 350 amphibian species (Fisher, Garner, & Walker, 2009).

The spread of this fungus has been linked to several anthropogenic factors including climate change. However, the main driver appears to be the global trade of amphibians that act as reservoirs from which the disease may spread into wild populations (Dunn & Hatcher, 2015). Another example of the devastating effects of non‐native pathogens on a native community is the crayfish plague.

The crayfish plague, caused by the fungus Aphanomyces astaci, was introduced in Europe by the invasive signal crayfish (Pacifastacus leniusculus). This introduction has led to the extinctions of the local populations of the native white‐clawed crayfish (Austropotamobius pallipes) (Dunn & Hatcher, 2015; Holdich & Poeckl, 2007).

Although pathogens can cause local extinction of new hosts in the new range, they often rely on the original reservoir (i.e., host) for their persistence.

For example, an outbreak of crayfish plague in Ireland, which does not harbor the signal crayfish, led to rapid local decline of the native crayfish, but the fungus also died out (Dunn & Hatcher, 2015; Reynolds, 1988). Besides threats to animals, also humans are at risk when non‐native pathogens enter the native community. Tick‐borne encephalitis (TBE) is a human viral infectious disease caused by the tick‐borne encephalitis virus (TBEV).

The virus is transmitted by the bite of infected ticks (mainly Ixodes ricinus in Europe), but humans can also acquire infection by consumption of contaminated unpasteurized dairy products. A number of biotic (e.g., host species and diversity) and abiotic (e.g., temperature, rainfall, humidity) factors may influence the presence of infected ticks and contribute to an increase in the incidence of TBE in Europe during the last decades (Heylen, Tijsse, Foncille, Matthysen, & Sprong, 2013).

Another potential threat for humans is mosquito‐borne diseases. Aedes aegypti is a mosquito that acts as a vector for viruses, for example, causing Zika, dengue, and chikungunya. Over a million people die each year from these diseases. The changing distribution of vectors and vectored pathogens is a new global health threat (Medlock et al., 2012; Singer, 2017). Although the mosquito is of African origin, it has dispersed to tropical and subtropical areas outside of Africa. Changing climate has facilitated its dispersal to new areas that were previously uninhabitable. This mosquito is now more widely dispersed than at any point in the past and will spread rapidly throughout the world in the near future, as the planet continues to warm (Khormi & Kumar, 2014; Singer, 2017).

Over the past few years, a new set of microbes frozen in time has emerged in laboratories: frozen banks of healthy donors’ gut microbes that are used in therapeutic fecal microbiota transplants (FMT). Studies on the role of gut microbes in human health are currently booming, revealing strong associations between gut microbiota dysbioses and diverse diseases, from inflammatory bowel disease and obesity to Parkinson’s and Alzheimer’s diseases (Belkaid & Hand, 2014).

New therapies, based on fecal transplants (i.e., the administration of fecal material from a donor into the gastrointestinal tract of a recipient, via nasogastric tube, enema, colonoscopy, or oral capsules, to change the recipient’s microbial composition), are now envisaged to prevent or cure such diseases (Gupta, Allen‐Vercoe, & Petrof, 2016; Hamilton, Weingarden, Unno, Khoruts, & Sadowsky, 2013).

While FMT were initially performed with fresh fecal slurries, they now also successfully use standardized, partially purified, and frozen fecal microbiota (Hamilton et al., 2013). FMT proved, for instance, to be a highly effective therapy for recurrent Clostridium difficile infections, whose incidence and severity have increased markedly since the 1990s, with frequent failure of standard antibiotic treatments (Hamilton et al., 2013; Weil & Hohmann, 2015).

Despite their efficiency and their high therapeutic potential, FMT should be used with caution, as we still have little perspective on their long‐term effects (Weil & Hohmann, 2015). Beyond the evident risk of pathogens transmission, which can be limited by an attentive screening of stool samples (Gupta et al., 2016; Weil & Hohmann, 2015), FMT may have unexpected side effects, such as the stimulation of chronic diseases (e.g., obesity, diabetes, and atherosclerosis) or behavioral disorders in the recipient patient (Gupta et al., 2016).

Indeed, evidence has accumulated that the gut microbiota is a complex community that interacts with numerous aspects of host physiology and behavior, including processes once thought to depend mainly on the host genetic program, such as development, immunity, metabolism, and the functioning of the brain (Macke, Tasiemski, Massol, Callens, & Decaestecker, 2017).

In both mice and humans, the gut microbiota structure was shown to differ between lean and obese individuals (Sommer & Bäckhed, 2013; Turnbaugh et al., 2006), and reciprocal FMT between monozygotic twins discordant for their body mass index revealed the transmissibility and reversibility of the obese phenotype (Ridaura et al., 2013).

Germ‐free mice receiving the stool from an obese donor developed greater adiposity than those colonized with a “lean” microbiota (Ridaura et al., 2013; Turnbaugh et al., 2006), revealing that FMT can have a huge impact on the metabolism of the recipient host. Transplant studies further highlighted a role for the gut microbiota in modulating stress responses and behaviors related to psychiatric disorders, such as anxiety and depression (Dinan & Cryan, 2015).

Such effects thus need to be accounted for when choosing the donors for FMT. To illustrate this, Alang and Kelly (2015) recently reported a case of a woman successfully treated with FMT for recurrent Clostridium difficile infection, who developed new‐onset obesity after receiving stool from a healthy, but overweight donor.

Other factors, such as genetics, ethnicity, and age, may also be important to consider when choosing a donor. Indeed, there is evidence that host genetics influence the structure of the gut microbiota (Goodrich et al., 2014) and that human populations from different countries, with different environments and lifestyles, have differences in the functional structure of their gut microbiome.

The structure of the gut microbiota also varies with age, and it has been hypothesized that specific microbial genes that are beneficial early in life may be harmful later in life, as exemplified by the bacterium Helicobacter pylori which improves control of infection and allergy early in life but promotes atrophy and oncogenesis later on (Cho & Blaser, 2012; Lin & Koskella, 2014).

When performing FMT, some donors may thus be more compatible than others with a given recipient patient. Taken together, these data suggest that the choice of the donor is crucial, which questions the appropriateness of universal frozen stool banks.

Alien pathogens can be transported and subsequently introduced through a range of pathways. Some will successfully establish and persist within hosts present within the introduced range and, furthermore, some will spread with the potential to threaten wildlife or humans.

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