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. Human activities and their effects on the climate and environments, such as the deep subsurface and ‘extreme’ Habitats Environments in which an environment cause unprecedented animal and plant environments. Microorganisms date back to the origin 1–4 organism normally lives; for extinctions, cause loss in biodiversity and endanger of life on Earth at least 3.8 billion years ago, and they example, lake, forest, sediment animal and plant life on Earth5. Losses of species, com- will likely exist well beyond any future extinction events. and polar environments munities and habitats are comparatively well researched, Although microorganisms are crucial in regulat- represent distinct types of 6 habitats. documented and publicized . By contrast, microorgan- ing climate change, they are rarely the focus of climate isms are generally not discussed in the context of cli- change studies and are not considered in policy devel- Ecosystem mate change (particularly the effect of climate change opment. Their immense diversity and varied responses The interacting community of on microorganisms). While invisible to the naked eye to environmental change make determining their role in organisms and non- living and thus somewhat intangible7, the abundance (~1030 the ecosystem challenging. In this Consensus Statement, components such as minerals, 8 nutrients, water, weather and total bacteria and archaea) and diversity of microorgan- we illustrate the links between microorganisms, macro- topographic features present in isms underlie their role in maintaining a healthy global scopic organisms and climate change, and put humanity a specific environment. ecosystem: simply put, the microbial world constitutes on notice that the microscopic majority can no longer the life support system of the biosphere. Although be the unseen elephant in the room. Unless we appreciate human effects on microorganisms are less obvious and the importance of microbial processes, we fundamen- certainly less characterized, a major concern is that tally limit our understanding of Earth’s biosphere and changes in microbial biodiversity and activities will response to climate change and thus jeopardize efforts affect the resilience of all other organisms and hence to create an environmentally sustainable future6 (BOx 1). their ability to respond to climate change9. Microorganisms have key roles in carbon and nutri- Scope of the Consensus Statement *e- mail: r.cavicchioli@ ent cycling, animal (including human) and plant health, In this Consensus Statement, we address the effects of unsw.edu.au agriculture and the global food web. Microorganisms live microorganisms on climate change, including micro- https://doi.org/10.1038/ in all environments on Earth that are occupied by macro- bial climate- active processes and their drivers. We also s41579-019-0222-5 scopic organisms, and they are the sole life forms in other address the effects of climate change on microorganisms, NATURE REVIEWS | MICROBIOLOGY VOLUME 17 | SEPTEMBER 2019 | 569 CONSENSUS STATEMENT Food web focusing on the influences of climate change on micro- terrestrial) that highlight the effects of climate change Interconnecting components bial community composition and function, physio- on microbial processes and the consequences. We also describing the trophic (feeding) logical responses and evolutionary adaptation. Although highlight agriculture and infectious diseases and the role interactions in an ecosystem, we focus on microorganism–climate connections, of microorganisms in climate change mitigation. Our often consisting of multiple food chains; for example, human activities with a less direct but possibly syner- Consensus Statement alerts microbiologists and non- marine microbial primary gistic effect, such as via local pollution or eutrophication, microbiologists to address the roles of microorganisms in producers and heterotrophic are also addressed. accelerating or mitigating the impacts of anthropogenic remineralizers through to the For the purpose of this Consensus Statement, we climate change (BOx 1). highest trophic predators or define ‘microorganism’ as any microscopic organism or trees as primary producers, herbivores and microbial virus not visible to the naked eye (smaller than 50 μm) Marine biome nitrogen fixers and that can exist in a unicellular, multicellular (for exam- Marine biomes cover ~70% of Earth’s surface and range remineralizers. ple, differentiating species), aggregate (for example, from coastal estuaries, mangroves and coral reefs to the biofilm) or viral form. In addition to microscopic bac- open oceans (Fig. 1). Phototrophic microorganisms use Subsurface water column The area below Earth’s surface, teria, archaea, eukaryotes and viruses, we discuss cer- the sun’s energy in the top 200 m of the , with subsurface ecosystems tain macroscopic unicellular eukaryotes (for example, whereas marine life in deeper zones uses organic and extending down for several larger marine phytoplankton) and wood- decomposing inorganic chemicals for energy10. In addition to sun- kilometres and including fungi. Our intent is not to exhaustively cover all envi- light, the availability of other energy forms and water terrestrial deep aquifer, ronments nor all anthropogenic influences but to pro- temperature (ranging from approximately −2 °C in ice- hydrocarbon and mine systems, biomes and marine sediments and the vide examples from major global (marine and covered seas to more than 100 °C in hydrothermal vents) ocean crust. Eutrophication Author addresses Increased input of minerals and 1School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, NSW, Australia. nutrients to an aquatic system; 2Department of Forest Ecosystems and Society, Oregon State University, Corvallis, OR, USA. typically nitrogen and 3Institute of Microbiology, Technical University Braunschweig, Braunschweig, Germany. phosphorus input from 4 fertilizers, sewage and Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA, USA. 5 detergents. Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås, Norway. 6Institute of Infection and Global Health, University of Liverpool, Liverpool, UK. Phytoplankton 7Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, USA. Single- celled, chlorophyll- 8Alfred Wegener Institute, Helmholtz Center for Marine and Polar Research, Bremerhaven, Germany. containing microorganisms 9Max Planck Institute for Marine Microbiology, Bremen, Germany. (eukaryotes and bacteria) that 10Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS, Australia. grow photosynthetically and 11Rubenstein School of Environment and Natural Resources, and The Gund Institute for Environment, University of Vermont, drift relatively passively with Burlington, VT, USA. the current in oceans or lakes. 12Institute of Integrative Biology, ETH Zurich, Zurich, Switzerland. 13 Biomes Department of Life and Environmental Sciences, Polytechnic University of Marche, Ancona, Italy. Systems containing multiple 14Stazione Zoologica Anton Dohrn, Naples, Italy. ecosystems that have common 15Center for Biofilm Engineering, and Chemical and Biological Engineering Department, Montana State University, physical properties (such as Bozeman, MT, USA. climate and geology); here 16Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, ‘biome’ is used to refer to all Amsterdam, Netherlands. terrestrial environments 17Department of Biological Sciences, Marine and Environmental Biology Section, University of Southern California, (continents) and all marine Los Angeles, CA, USA. environments (seas and 18 oceans). Biological Sciences Division, Earth and Biological Sciences Directorate, Pacific Northwest