Back to the future in a petri dish: Origin and impact of resurrected microbes in natural populations

Abstract

Current natural populations face new interactions because of the re‐emergence of ancient microbes and viruses. These risks come from the re‐emergence of pathogens kept in laboratories or from pathogens that are retained in the permafrost, which become available upon thawing due to climate change. We here focus on the effects of such re‐emergence in natural host populations based on evolutionary theory of virulence and long‐term studies, which investigate host–pathogen adaptations. Pathogens tend to be locally and temporally adapted to their co‐occurring hosts, but when pathogens from a different environment or different time enter the host community, the degree to which a new host–pathogen interaction is a threat will depend on the specific genotypic associations, the time lag between the host and the pathogen, and the interactions with native or recent host and pathogen species. Some insights can be obtained from long‐term studies using a resurrection ecology approach. These long‐term studies based on time‐shift experiments are essential to obtain insight into the mechanisms underlying host–pathogen coevolution at several ecological and temporal scales. As past pathogens and their corresponding host(s) can differ in infectivity and susceptibility, strong reciprocal selective pressures can be induced by the pathogen. These strong selective pressures often result in an escalating arms race, but do not necessarily result in increased infectivity over time. Human health can also be impacted by these resurrected pathogens as the majority of emerging infectious diseases are zoonoses, which are infectious diseases originating from animal populations naturally transmitted to humans. The sanitary risk associated with pathogen emergence from different environments (spatial or temporal) depends on a combination of socioeconomic, environmental, and ecological factors that affect the virulence or the pathogenic potential of microbes and their ability to infect susceptible host populations.

Analysing eco‐evolutionary dynamics—The challenging complexity of the real world

“…The resurrection ecology approach (Decaestecker et al, ; Franks, Hamann, & Weis, ; Stoks, Govaert, Pauwels, Jansen, & Meester, ; Sultan, Horgan‐Kobelski, Nichols, Riggs, & Waples, ) applied to multiple species simultaneously might provide a powerful way to obtain insight into the impact of evolution as it occurred in nature on ecological processes. Here, again one could test the impact of evolution of every species separately and in combination, and carry out “transplants” over time (Houwenhuyse, Macke, Reyserhove, Bulteel, & Decaestecker, ; Penczykowski et al, 2015), replacing evolved populations by representatives of their ancestors either for the whole community or for each of the member species, and quantify its feedback on ecological processes. Resurrection ecology can be applied on layered archives of dormant stages (mainly in aquatic systems, e.g., Stoks et al, ) or when dormant stages have been collected at different moments of a population's history (Franks et al, ). Field transplants with adapted/nonadapted species sets .…”

Evolutionary aspects of resurrection ecology: Progress, scope, and applications—An overview

“…This involves resuscitation of ancestral populations from either natural populations (e.g., collected from sediment cores) or archived populations (e.g., seed bank collections) and then comparing these ancestral lineages to modern‐day descendants. Many of the contributions to this special issue take a “back‐in‐time” approach and focus on specific model organisms (e.g., Artemia —Lenormand et al., ; bacteria—Houwenhuyse, Macke, Reyserhove, Bulteel, & Decaestecker, ; Shoemaker & Lennon, ; Daphnia —Goitom et al., ; Cuenca Cambronero, Bettina, & Orsini, ; phytoplankton—Ellegaard, Godhe, & Riberio, ). However, as pointed out in the contribution from Franks et al., ; this issue), a “forward‐in‐time” approach (a.k.a.…”

“…Much of this reduction in hatching success is due to natural aging of these propagules in sediments that may be anoxic or even toxic (i.e., hydrogen sulfide—H 2 S; Weider et al., ). Thus, to this point in time, retrieving and reviving large numbers of propagules for most organisms (i.e., see exceptions for phytoplankton—Ellegaard et al., and microbes—Houwenhuyse et al., ; Shoemaker & Lennon, ) that date back much more than 70‐100 years remains challenging (Burge et al., ; Ellegaard et al., ; Frisch et al., ; Morton et al., ). Given the current rate of environmental change, and given what we know about contemporary evolution (e.g., Franks, Hamann, and Weis, this issue), even a 70‐ to 100‐year time span can represent enough spent generations (particularly, for short‐lived organisms), to allow sufficient time to track evolutionary changes, and thus, provide valuable insights into the evolutionary processes in both pristine and human‐impacted populations.…”

“…Other applied aspects of RE that are represented by contributions to this special issue, and that are important in understanding the ecology and evolution of natural populations and communities include (i) invasive species biology (i.e., Artemia —Lenormand et al., ); (ii) the role of RE in possible pathogen–host interactions that impact both human and nonhuman populations via “dispersal from the past” (i.e., melting permafrost releasing microbial pathogens—Houwenhuyse et al., ); (iii) climate and land‐use changes impacting nutrient enrichment (i.e., eutrophication of aquatic systems—Ellegaard et al., ; Cuenca Cambronero et al., ); and (iv) evolutionary feedback and ecosystem functioning (i.e., Goitom et al., ).…”

“…Another contribution by Houwenhuyse et al. () provides a review of the potential “dispersal from the past” of potential pathogens, and how re‐emergence of ancient microbes and viruses may pose risks to modern‐day hosts. Recent examples of the release of active pathogens from Arctic permafrost (e.g., anthrax from 75‐year‐old reindeer carcasses in Russia) due to climate change raise an important applied aspect of RE related to human health and nonhuman disease epidemiology.…”