key: cord-0005461-qfqku5kh authors: Huang, Li; Xiao, Xiang; Zhao, Guoping title: Microbes: the hidden giant behind the biogeochemical cycling of elements in the hydrosphere date: 2019-09-27 journal: Sci China Life Sci DOI: 10.1007/s11427-019-1554-y sha: 74df0e535146f30e8c891097674cf0c25370d38d doc_id: 5461 cord_uid: qfqku5kh nan Microbes are the oldest inhabitants of Earth. Through billions of years of coevolution with Earth, these creatures, usually invisible to the naked eye, have contributed to shaping the Earth surface, creating an ecosystem habitable for higher organisms including humans. By some estimates, microbes account for up to half of the biomass on the planet today (Whitman et al., 1998) . They thrive in every corner of Earth, including harsh habitats such as hot springs, hydrothermal vents, salt and soda lakes, acid mine drainage, deep subsurface, and thus define the boundaries of the biosphere. Microbes also exhibit immense genetic and metabolic diversity. Therefore, it is not surprising that these organisms play a pivotal role in driving elemental cycling on Earth, a process essential for maintaining the habitability of the planet Earth. About 3/4 of the Earth surface is covered with water, and the hydrosphere comprising oceans, lakes, rivers, glaciers, wetlands, groundwater, etc. is home to over half of the microbes on Earth. It is increasingly being recognized that microbial activity in the hydrosphere has a great impact on the Earth ecosystem. For example, one half of the O 2 that we breathe comes from the oceans, and about half of the CO 2 generated by human activities is absorbed by the oceans. Over half of the CH 4 , a greenhouse gas, is produced in wetlands, marshes and paddy fields. N 2 fixed in the oceans accounts for 2/3 of the naturally fixed N 2 . 30% of atmospheric N 2 O, another greenhouse gas, is released from the oceans. Microbes are clearly a hidden giant driving these diverse and fundamental biogeochemical processes in the hydrosphere. Thanks to the rapid progress in sequencingbased technologies and significant improvement in sampling, cultivation and analytical capabilities, our knowledge of the roles of microbes in elemental cycling in the hydrosphere has been expanded dramatically in the past two decades. The new field of geomicrobiology has attracted fast growing research interests. Some long-held concepts have been shattered by the discoveries of novel microbes and novel metabolic pathways. For example, novel anaerobic methanotrophic archaea (ANME) were found to oxidize methane in cooperation with sulfate reducing bacteria (Hinrichs et al., 1999) . This reaction is believed to help prevent the release of vast amounts of CH 4 stored beneath the seafloor into the atmosphere. A group of bacteria of the phylum Planctomycetes were shown to be capable of anaerobic ammonium oxidation, a novel pathway in nitrogen cycle (Strous et al., 1999) . Previous to this finding, ammonium oxidation was thought to occur only under aerobic conditions. Anaerobic ammonium oxidation is responsible for the loss of~50% of the nitrogen compounds from the oceans in the form of N 2 . Despite the remarkable progress, a huge knowledge gap remains in our understanding of the roles of microbes in driving elemental cycling in the hydrosphere. The vast majority of the microbes in the environment still evade cultivation, not to mention further functional studies. Therefore, it is anticipated that this flourishing field will continue to produce fascinating new discoveries in years to come. China has been an active player in geomicrobiological research and has made important contributions to the understanding of the biogeochemical roles of microbes in various aquatic habitats. In 2016, the National Natural Science Foundation of China launched a major research program titled "Mechanisms underlining elemental cycling on Earth by microorganisms in the hydrosphere" (or "Hydrosphere Microbes") (Huang et al., 2017) . This Program aims to learn how microbes carry out carbon, nitrogen and sulfur cycling at the cellular, community and ecological levels in representative aquatic habitats, including oceans, estuaries, lakes, wetlands, and extreme aquatic environments, through joint efforts by scientists in life sciences, earth sciences, chemical sciences, information sciences, etc. Knowledge gained through the implementation of the Program will enhance our ability to predict and respond to the impact of environmental changes on the Earth ecosystem. In this issue, we compiled one research paper and three review articles authored by well-known experts in the field. These articles are intended to offer a taste of excitement that might come out of the research entailed in the Program. Much of the emphasis of the Program is placed on oceans, where microbial activities are known to exert a huge impact on the Earth ecosystem. For example, anaerobic oxidation of methane (AOM), which occurs predominantly in oceans, plays a key role in controlling global methane emission. Coupling of AOM with sulfate reduction has been extensively characterized. Over the years, AOM has also been shown to be coupled with the reduction of other external electron acceptors such as manganese and iron (Beal et al., 2009; Scheller et al., 2016) . However, metabolic mechanisms involved in these processes remain largely unknown. In this issue, Liang et al. reviewed geochemical evidence for metal-dependent AOM in various marine environments and discussed the possible biochemical mechanisms in the processes (Liang et al., 2019) . The biogenic trace gas dimethyl sulfide (DMS) is the dominant natural source of volatile organic sulfur compounds emitted into the atmosphere from the marine environment. DMS is mainly produced by the enzymatic cleavage of dimethylsulfoniopropionate (DMSP) (Curson et al., 2011) . Both DMS and DMSP play important roles in driving the global sulfur cycle and thus may affect climate. It was long believed that only marine eukaryotes such as phytoplankton could produce DMSP. However, the authors of a review article (Zhang et al., 2019) in this issue recently discovered that marine heterotrophic bacteria also produced DMSP (Curson et al., 2017) . In the review, they describe the global distribution pattern of DMSP and DMS, the relative contributions of marine phytoplankton and bacteria to the production of DMSP and its degradation to DMS, and the physiological and ecological functions of these important organosulfur molecules to permit a better understanding of the mechanisms of DMSP and DMS production and their roles in the environment (Zhang et al., 2019) . Microbes in aquatic environments other than oceans also serve unique biogeochemical roles. Microbial community structures and activities in lakes have attracted substantial research interests in recent years. However, a biogeographic distribution pattern in global lakes and its controlling factors have not been fully disclosed. In their research article, Yang et al. compiled and analyzed a large number of environmental 16S rRNA sequences from 431 lakes across a wide range of geographical distance and environmental conditions. Their work allows a better understanding of the impact of geographic distance, environmental conditions, and stochastic processes on microbial distribution in global lakes . Microbes are able to exchange electrons between cells (Shi et al., 2016; Summers et al., 2010) . Electron exchanges between the quinol/quinone pools in microbial cytoplasmic membrane and extracellular substrates are known as microbial extracellular electron transfer (EET). Microbes with EET capabilities are widespread in the hydrosphere, such as sediments of rivers, lakes and oceans, where they play crucial roles in biogeochemical cycling of key elements, including carbon, nitrogen, sulfur, iron and manganese (Kappler and Bryce, 2017; Myers and Nealson, 1988; Nielsen et al., 2010) . In this issue, Jiang et al. review the molecular mechanisms underlying the microbial ability for extracellular redox transformation of iron, direct interspecies electron transfer as well as long distance electron transfer mediated by the cable bacteria in the hydrosphere . Obviously, areas of research covered in this collection of articles represent only a very small fraction of those in the Program-sponsored projects. The ultimate goal of the Program is to improve the picture of the biogeochemical roles of microbes in the hydrosphere. Dr. Li Huang received his Ph.D. from the University of Guelph, Canada, in 1988 . From 1988 to 1993 Manganese-and irondependent marine methane oxidation Dimethylsulfoniopropionate biosynthesis in marine bacteria and identification of the key gene in this process Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes Methane-consuming archaebacteria in marine sediments Focusing on key scientific issues of microbiome research in hydrosphere: NSFC major research plan for microbes in hydrosphere Molecular underpinnings for microbial extracellular electron transfer during biogeochemical cycling of earth elements Cryptic biogeochemical cycles: unravelling hidden redox reactions Metal-dependent anaerobic methane oxidation in marine sediment: insights from marine settings and other systems Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor Electric currents couple spatially separated biogeochemical processes in marine sediment Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction Extracellular electron transfer mechanisms between microorganisms and minerals Missing lithotroph identified as new planctomycete Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria Prokaryotes: the unseen majority A comprehensive census of lake microbial diversity on a global scale Biogenic production of DMSP and its degradation to DMS-their roles in the global sulfur cycle