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Chinese Science Bulletin, Volume 63 , Issue 36 : 3911-3919(2018) https://doi.org/10.1360/N972018-00612

Viruses in the deep biosphere: A review

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  • ReceivedJun 21, 2018
  • AcceptedJul 31, 2018
  • PublishedAug 27, 2018

Abstract

Viruses, the most abundant biological entities on the planet, are widely distributed in various environments, including the deep biosphere. Via infection, which is frequently followed by lysis of the host cells, viruses play an important role in shaping microbial population structure, impacting the ecological characteristics of their hosts, and breaking up cellular biomass into organic matter, thereby affecting microbial processes and nutrient cycling. Because of these activities, viruses are known as nano-scale drivers of global-scale processes. The deep biosphere, extending hundreds to thousands of meters below the seafloor, harbors by far the largest reservoir of organic carbon and more than half of the world's prokaryotic organisms. However, it remains a "black box" in terms of the ecological characteristics and functions of its resident viruses. To date, only a few studies on viruses in the deep biosphere have been reported, and these mainly originate from the Ocean Drilling Program (ODP) and the Integrated Ocean Drilling Program (IODP). The limited results of these studies show that the abundance of viruses in the deep biosphere is much greater than that in marine environments (108–109 viruses g-1 in sediments versus 106–108 viruses mL-1 in seawater). In general, viral abundance decreases with an increase in depth, but the Virus-to-Prokaryote Ratio, which is used to predict the relationship between viral and prokaryotic communities, varies greatly among different deep habitats. Viral abundance is affected not only by in situ viral production and decay, processes that are usually tightly linked to the productivity of microbial hosts and the activity of extracellular enzymes, but also by the physical, chemical, and geological characteristics of the environment, including temperature, total organic carbon content, sediment porosity, and sedimentation rate, amongst other factors. In addition, virus assemblages in the deep biosphere appear to be both morphologically and genetically more diverse than their aquatic counterparts. Highly diverse morphotypes and unknown virus sequences indicate that there is a huge uncharacterized viral pool in the deep biosphere, which could represent a treasure trove for the future discovery of novel viruses and lifestyle mechanisms. In addition, analyses of prophage sequences deduced from prokaryotic genomes imply that lysogenic infection should be an important life strategy for viruses, making them more adaptable to the dynamic, and often extreme, deep biosphere environment. These findings have important implications for the potential interactions between viruses and their hosts and for the vital role of viruses in manipulating microbial community structure and evolution in the deep biosphere. However, technical difficulties, which have only recently been at least partially overcome, have limited our ability to study these elusive viruses. The fact is that we have barely begun to characterize the deep virosphere, which is the "dark matter" of the biological world and a tremendous source of future discoveries. The questions of what role viruses play in the deep biosphere, whether and to what extent viruses drive the metabolic functioning and evolution of microbial populations, and how virus populations adapt to deep environments are still open and answering them will require significant amounts of work. The purpose of this review is, therefore, to provide an overview of the current knowledge about viruses (e.g., distribution, diversity, and life cycles) in the deep biosphere. The relationships of viruses with microbial hosts and environmental parameters and the potential ecological importance of viruses in the deep biosphere are discussed. Finally, we put forward some suggestions regarding areas of research that need to be addressed in the future to establish a more complete picture of the ecological and evolutionary significance of viruses in the biosphere.


Funded by

国家自然科学基金(41522603)

国家自然科学基金(31570172)

青岛海洋科学与技术国家实验室项目(QNLM2016ORP0303)

中国大洋矿产资源研究开发协会项目(DY135-E2-1-04)


Acknowledgment

感谢中国科学院微生物研究所黄力研究员、中国地质大学(北京)董海良教授和中国地质大学(武汉)谢树成教授的建议和讨论.


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  • Figure 1

    Sampling sites for virus research in deep biosphere. Voyage(Sites): ODP Leg 169S(1033B, 1034B)[9]; IODP 307(U1317)[10]; ODP Leg 201(1225, 1226, 1227, 1228, 1229, 1230, 1231)[11]; IODP 329(U1365, U1366, U1367, U1368, U1369, U1370, U1371), IODP 323(U1344)[13]; ODP Leg 204(1251), IODP 308(U1320A, U1320B)[12]; IODP 327(1364A, 1362B)[14]. Picture made by Ocean Data View(ODV)

  • Figure 2

    Abundance of viruses (a) and prokaryotes (b) and VPR (c) in deep biosphere. Data from that surface sediment of the Subtropical Pearl River Estuary(diamond)[16], ODP Leg 201[11], IODP Exp 329, IODP Leg 323[13], ODP Leg 204, U1320A, U1324B, C9001[12], IODP 327[14]

  • Figure 3

    Morphologies of viruses observed in basalt-hosted crustal fluid. (a–h) Electron micrographs of particles harvested from borehole U1362A revealed tailed viruses similar to members of the order Caudovirales (a and b), untailed viruses (c), lemon-shaped viruses resembling members of the family Bicaudaviridae or Fuselloviridae (d), rod-shaped viruses resembling members of the family Rudiviridae (e), and other particles resembling filamentous (f) or spindle-shaped (g) viruses isolated from Archaea. Bilobate structures in the viral size range (h) were repeatedly observed, but they were unlike any classified viruses. These might represent a novel virus or may be membrane vesicles. Bars, 100 nm[14]

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