Scientists’ warning to humanity: microorganisms and climate change

CONSENSuS Statement Scientists’ warning to humanity: microorganisms and climate change Ricardo Cavicchioli 1*, William J. Ripple2, Kenneth N. Timmis3, Farooq Azam4, Lars R. Bakken5, Matthew Baylis 6, Michael J. Behrenfeld7, Antje Boetius 8,9, Philip W. Boyd10, Aimée T. Classen11, Thomas W. Crowther12, Roberto Danovaro13,14, Christine M. Foreman 15, Jef Huisman 16, David A. Hutchins17, Janet K. Jansson 18, David M. Karl 19, Britt Koskella 20, David B. Mark Welch 21, Jennifer B. H. Martiny22, Mary Ann Moran 23, Victoria J. Orphan24, David S. Reay25, Justin V. Remais 26, Virginia I. Rich 27, Brajesh K. Singh 28, Lisa Y. Stein 29, Frank J. Stewart30, Matthew B. Sullivan 31, Madeleine J. H. van Oppen 32,33, Scott C. Weaver34, Eric A. Webb17 and Nicole S. Webster 33,35 Abstract | In the Anthropocene, in which we now live, climate change is impacting most life on Earth. Microorganisms support the existence of all higher trophic life forms. To understand how humans and other life forms on Earth (including those we are yet to discover) can withstand anthropogenic climate change, it is vital to incorporate knowledge of the microbial ‘unseen majority’. We must learn not just how microorganisms affect climate change (including production and consumption of greenhouse gases) but also how they will be affected by climate change and other human activities. This Consensus Statement documents the central role and global importance of microorganisms in climate change biology. It also puts humanity on notice that the impact of climate change will depend heavily on responses of microorganisms, which are essential for achieving an environmentally sustainable future. Habitats Environments in which an organism normally lives; for example, lake, forest, sediment and polar environments represent distinct types of habitats. Ecosystem The interacting community of organisms and non-living components such as minerals, nutrients, water, weather and topographic features present in a specific environment. *e-mail: r.cavicchioli@ unsw.edu.au https://doi.org/10.1038/ s41579-019-0222-5 Human activities and their effects on the climate and environment cause unprecedented animal and plant extinctions, cause loss in biodiversity1–4 and endanger animal and plant life on Earth5. Losses of species, communities and habitats are comparatively well researched, documented and publicized6. By contrast, microorganisms are generally not discussed in the context of climate change (particularly the effect of climate change on microorganisms). While invisible to the naked eye and thus somewhat intangible7, the abundance (~1030 total bacteria and archaea)8 and diversity of microorganisms underlie their role in maintaining a healthy global ecosystem: simply put, the microbial world constitutes the life support system of the biosphere. Although human effects on microorganisms are less obvious and certainly less characterized, a major concern is that changes in microbial biodiversity and activities will affect the resilience of all other organisms and hence their ability to respond to climate change9. Microorganisms have key roles in carbon and nutrient cycling, animal (including human) and plant health, agriculture and the global food web. Microorganisms live in all environments on Earth that are occupied by macroscopic organisms, and they are the sole life forms in other NATuRe RevIeWS | MiCrobiology environments, such as the deep subsurface and ‘extreme’ environments. Microorganisms date back to the origin of life on Earth at least 3.8 billion years ago, and they will likely exist well beyond any future extinction events. Although microorganisms are crucial in regulating climate change, they are rarely the focus of climate change studies and are not considered in policy development. Their immense diversity and varied responses to environmental change make determining their role in the ecosystem challenging. In this Consensus Statement, we illustrate the links between microorganisms, macroscopic organisms and climate change, and put humanity on notice that the microscopic majority can no longer be the unseen elephant in the room. Unless we appreciate the importance of microbial processes, we fundamentally limit our understanding of Earth’s biosphere and response to climate change and thus jeopardize efforts to create an environmentally sustainable future6 (Box 1). Scope of the Consensus Statement In this Consensus Statement, we address the effects of microorganisms on climate change, including microbial climate-active processes and their drivers. We also address the effects of climate change on microorganisms, volume 17 | SEPTEMBER 2019 | 569 C o n S e n S u S S tat e m e n t Food web Interconnecting components describing the trophic (feeding) interactions in an ecosystem, often consisting of multiple food chains; for example, marine microbial primary producers and heterotrophic remineralizers through to the highest trophic predators or trees as primary producers, herbivores and microbial nitrogen fixers and remineralizers. Subsurface The area below Earth’s surface, with subsurface ecosystems extending down for several kilometres and including terrestrial deep aquifer, hydrocarbon and mine systems, and marine sediments and the ocean crust. Eutrophication Increased input of minerals and nutrients to an aquatic system; typically nitrogen and phosphorus input from fertilizers, sewage and detergents. Phytoplankton Single-celled, chlorophyll- containing microorganisms (eukaryotes and bacteria) that grow photosynthetically and drift relatively passively with the current in oceans or lakes. Biomes Systems containing multiple ecosystems that have common physical properties (such as climate and geology); here ‘biome’ is used to refer to all terrestrial environments (continents) and all marine environments (seas and oceans). Phototrophic Using sunlight to generate energy for growth. Water column The water layer in a lake or ocean. focusing on the influences of climate change on microbial community composition and function, physio logical responses and evolutionary adaptation. Although we focus on microorganism–climate connections, human activities with a less direct but possibly synergistic effect, such as via local pollution or eutrophication, are also addressed. For the purpose of this Consensus Statement, we define ‘microorganism’ as any microscopic organism or virus not visible to the naked eye (smaller than 50 μm) that can exist in a unicellular, multicellular (for example, differentiating species), aggregate (for example, biofilm) or viral form. In addition to microscopic bacteria, archaea, eukaryotes and viruses, we discuss certain macroscopic unicellular eukaryotes (for example, larger marine phytoplankton) and wood-decomposing fungi. Our intent is not to exhaustively cover all environments nor all anthropogenic influences but to provide examples from major global biomes (marine and terrestrial) that hig (...truncated)