Changes in the environmental microbiome in the Anthropocene

Abstract

In addition to changes in climate, land cover, biodiversity, and chemical composition, human activity is also inducing great changes in the microbial world. These changes are profoundly affecting the biogeochemical processes of the Earth, the global biology, and the human health, that is, they are influencing the sustainability of the Anthropocene. The Earth's surface is increasingly affected by human activity, from the loss of biodiversity to chemical pollution. Human impacts on the Earth ecosystem are so fundamental that a stratigraphic signature in sediments and ice has been produced. This has led to the proposal of a new geological epoch, the Anthropocene (Waters et al., 2016). The start of the early Anthropocene is marked by the spread of agriculture and deforestation, as well as large-scale species exchange. Technological revolutions in the mid-20th century fueled rapid population growth and industrialization, leading to diverse geochemical signatures, such as pollution from synthetic chemicals and metals, and enrichment of nutrients. In addition to changes in climate, land cover, biodiversity, and chemical composition, human activity is also inducing great changes in the microbial world (Figure 1). These changes are profoundly affecting biogeochemical processes in the Earth ecosystem and influencing the sustainability of the Anthropocene, but these alterations are poorly appreciated. The habitat disturbance, changes in substrates, and toxic effects of chemicals from human activity can directly influence the microbial world. Human activity can also affect the microbial world indirectly, for example, the extinction of plant and animal species may lead to the loss of microbial strains/taxa uniquely associated with species that have become extinct. Microbes are ubiquitous on Earth; they can be found even deep within the Earth. Both deep continental and oceanic subsurfaces may harbor about 60% of all the microbial cells in the entire biosphere (Flemming & Wuertz, 2019). Microorganisms can also be found in the air, even at high altitudes beyond the troposphere (Burrows, Elbert, & Lawrence, 2009). Microbial diversity is richest in soil, with each gram of soil potentially containing thousands of millions of microbial cells (Bardgett & Van Der Putten, 2014). Microbes have been essential in modulating the biogeochemistry and thus the chemical speciation of virtually all elements, so the current chemical composition and properties of our environment represent the integrated actions of microbes during the entire history of evolution on Earth. Microbes have also played an important role in human health throughout our history, for example, being responsible for infectious diseases and secondary microbial metabolites, such as antibiotics. Cataloguing the changes in environmental microbiomes while the Earth is experiencing unprecedented disturbance from anthropogenic activities is therefore necessary. However, in contrast to our general understanding of the role of microbiomes in biogeochemistry (e.g., how microbes mediate the generation of greenhouse gases) much less is known about how human activity is altering microbial diversity and functionality at multiple temporal and spatial scales. Earth's microbiomes are extremely diverse and highly redundant, which has hindered our understanding of these changes. The advent of molecular and genomic tools in recent decades is now enabling better characterization of microbial diversity. One example of the impact of the global change on Earth's microbiome is the impact of the input of reactive nitrogen (N) on Earth ecosystems and the responses of, and consequences to, the microbial engine. The invention of the Haber–Bosch process has greatly changed the dynamics of reactive nitrogen on Earth (Peñuelas, Jannssens, Ciais, Obersteiner, & Sardans, 2020; Peñuelas et al., 2013; Peñuelas, Sardans, Rivas-ubach, & Janssens, 2012). Anthropogenic input of reactive N is even evident in remote regions. An investigation of watersheds in a remote area of the Northern Hemisphere found that changes in the isotopic signature (15N/14N) of anthropogenic N input coincided with anthropogenic CO2 emissions and accelerated with the increasing industrial production of ammonium (Holtgrieve et al., 2011). The ever-increasing release of ammonium into the environment fuels the microbial engine by facilitating ammonium oxidation and then denitrification, leading to the release of nitrates to aquatic ecosystems and the emission of gaseous nitrous oxide to the air. The microbial world had never experienced such high levels of ammonium before the industrial production of ammonium, particularly in agroecosystems, and nitrifiers and denitrifiers in the Anthropocene are clearly playing a critical role in nitrogen biogeochemistry and thus environmental health. Many field studies have now documented the impact of anthropogenic inputs of N on microbial communities and their functional diversity. A study of soil in a buried Neolithic paddy (about 7,000 years old) in southeastern China found that modern agricultural practices have substantially shifted microbial functional diversity toward accelerated nutrient cycling, such as the biotransformation of N (Zhu et al., 2016). A 50 year fertilization experiment reported that the size of functional guilds involved in N cycling was greatly affected by N input, and the size of the functional guilds correlated well with corresponding biogeochemical processes (Hallin, Jones, Schloter, & Philippot, 2009). Tian et al. (2019) demonstrated that N deposition in a long-term experiment of tropical forest soil profoundly affected biogeochemical cycling by affecting the expression of microbial functional genes. This study identified important associations between the responses of soil microbial functional potentials and the cycling of soil nutrients (C, N, and P) to the anthropogenic input of N in “pristine” tropical forests. In addition to nutrient input, antimicrobial resistance (AMR) is a second example we would like to highlight. Antibiotics have been widely used and misused in the control of human infectious diseases and in intensive animal production since the discovery of penicillin, which has led to the emergence of AMR globally, in both clinical and general environments. AMR in the environment is ancient (D'Costa et al., 2011), but its emergence and spread in the environment are closely associated with the input of resistant microbes from humans and farm animals, as well as with the level of chemical pollution in the environment. Evidence in recent decades suggests a temporal increase in AMR in the environment. For example, an analysis of archived soils from the Netherlands from 1940 to 2008 found that alleles of genes conferring AMR have greatly increased in frequency since 1940, with some alleles >15-fold more abundant in 2008 than the 1970s (Knapp, Dolfing, Ehlert, & Graham, 2010). A continental survey of estuarine wetlands in China reported that wetland soils contained many AMR genes, and the number correlated well with anthropogenic factors in the river basin, such as population size, volume of discharge of waste water, and intensity of animal farming (Zhu, Gillings, et al., 2017). The impact of human activity on the microbial world is even evident in remote areas such as the high Arctic. A recent study found AMR genes in high Arctic soils, and the accumulation was more substantial in soils with elevated human impacts, indicated by relatively high phosphorus levels (McCann et al., 2019).. Environmental microbes and genes are traditionally studied in one location, or in one environmental compartment such as vegetation, the water column, or soil, with little attention paid to the dynamic exchange of microbes and genes across system boundaries and physical scales. For several thousands of millions of years, microorganisms and the genes they carry have primarily been moved by physical forces such as air and water currents, generating biogeographic patterns for microorganisms that humans have now significantly changed. We perturb microbial populations by transporting large numbers of cells to new locations, and by modifying selection pressures at those locations. As a consequence, we are substantially altering microbial biogeography (Zhu, Zhao, et al., 2017). Humans and farm animals now move on an unprecedented scale, and this movement actively transports and enriches a specific subset of microorganisms. Humans and farm animals now comprise 35-fold more biomass than wild terrestrial mammals (Smil, 2011), so the bacteria shed in feces mainly represent the gut microbiota of humans, cattle, sheep, goats, pigs, and chickens. The efficiency of microbial dispersal is enhanced by the 1.2 thousand of millions of international tourist movements per year, evidenced by the rapid spread of bacterial clones and genes conferring AMR between continents (Bengtsson-Palme et al., 2015). Humans also promote dispersal of microbial cells via mass movement of materials such as ballast water from commercial shipping, soil, sand and rock, and indirectly through erosion (Zhu, Gillings, et al., 2017). Microbial biogeography is further complicated by the ability of microorganisms to acquire foreign DNA, since movement of genes through ecosystems can also occur independently of organismal movement. DNA released from organisms can transfer to unrelated species either through close contact, or at a distance, when DNA can survive in the environment for extended time periods (Gillings, 2017). Incorporating all these changes through environmental genomics and elemental data into biogeochemical models will improve predictions about nutrient cycling (Mock et al., 2016; Reed, Algar, Huber, & Dick, 2014) and ecosystem functioning. Progress can only be made by forming new, interdisciplinary research teams that can manage and interpret the enormous data sets required. These data sets can then be applied to the complex, multigene phenotypes that are centrally important to global biogeochemistry and human health. Monitoring the environmental dissemination of genes, particularly those that confer phenotypes of direct relevance to human and animal health should now stimulate many more global questions. Investigations into microbial invasions, microbial extinctions, and perturbations to microbial ecosystems are now a high priority. In particular, monitoring and improvements of waste water and manure treatments are critical. Microorganisms usually perform their essential ecosystem services invisibly, but we ignore them at our peril. Earth's sustainability vitally depends on the interplay between microbes and all higher trophic life forms. As discussed above, the evidence that humans are leaving a deep footprint in the microbial world is now compelling, which will cause unprecedented disturbance to our environment, global biology, and human health. Including microbial processes in Earth System science and global change biology and human health, both as driving forces and as consequences of human disturbance, is therefore critical for understanding and managing planetary health.

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