A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes

Viral lysis of microbial hosts releases organic matter that can then be assimilated by nontargeted microorganisms. Quantitative estimates of virus-mediated recycling of carbon in marine waters, first established in the late 1990s, were originally extrapolated from marine host and virus densities, host carbon content and inferred viral lysis rates. Yet, these estimates did not explicitly incorporate the cascade of complex feedbacks associated with virus-mediated lysis. To evaluate the role of viruses in shaping community structure and ecosystem functioning, we extend dynamic multitrophic ecosystem models to include a virus component, specifically parameterized for processes taking place in the ocean euphotic zone. Crucially, we are able to solve this model analytically, facilitating evaluation of model behavior under many alternative parameterizations. Analyses reveal that the addition of a virus component promotes the emergence of complex communities. In addition, biomass partitioning of the emergent multitrophic community is consistent with well-established empirical norms in the surface oceans. At steady state, ecosystem fluxes can be probed to characterize the effects that viruses have when compared with putative marine surface ecosystems without viruses. The model suggests that ecosystems with viruses will have (1) increased organic matter recycling, (2) reduced transfer to higher trophic levels and (3) increased net primary productivity. These model findings support hypotheses that viruses can have significant stimulatory effects across whole-ecosystem scales. We suggest that existing efforts to predict carbon and nutrient cycling without considering virus effects are likely to miss essential features of marine food webs that regulate global biogeochemical cycles.     

Marine viruses--major players in the global ecosystem

Viruses are by far the most abundant 'lifeforms' in the oceans and are the reservoir of most of the genetic diversity in the sea. The estimated 10(30) viruses in the ocean, if stretched end to end, would span farther than the nearest 60 galaxies. Every second, approximately 10(23) viral infections occur in the ocean. These infections are a major source of mortality, and cause disease in a range of organisms, from shrimp to whales. As a result, viruses influence the composition of marine communities and are a major force behind biogeochemical cycles. Each infection has the potential to introduce new genetic information into an organism or progeny virus, thereby driving the evolution of both host and viral assemblages. Probing this vast reservoir of genetic and biological diversity continues to yield exciting discoveries.     

Will ocean acidification affect marine microbes?

The pH of the surface ocean is changing as a result of increases in atmospheric carbon dioxide (CO₂), and there are concerns about potential impacts of lower pH and associated alterations in seawater carbonate chemistry on the biogeochemical processes in the ocean. However, it is important to place these changes within the context of pH in the present-day ocean, which is not constant; it varies systematically with season, depth and along productivity gradients. Yet this natural variability in pH has rarely been considered in assessments of the effect of ocean acidification on marine microbes. Surface pH can change as a consequence of microbial utilization and production of carbon dioxide, and to a lesser extent other microbially mediated processes such as nitrification. Useful comparisons can be made with microbes in other aquatic environments that readily accommodate very large and rapid pH change. For example, in many freshwater lakes, pH changes that are orders of magnitude greater than those projected for the twenty second century oceans can occur over periods of hours. Marine and freshwater assemblages have always experienced variable pH conditions. Therefore, an appropriate null hypothesis may be, until evidence is obtained to the contrary, that major biogeochemical processes in the oceans other than calcification will not be fundamentally different under future higher CO₂/lower pH conditions.     

Biotic and Human Vulnerability to Projected Changes in Ocean Biogeochemistry over the 21st Century

Ongoing greenhouse gas emissions can modify climate processes and induce shifts in ocean temperature, pH, oxygen concentration, and productivity, which in turn could alter biological and social systems. Here, we provide a synoptic global assessment of the simultaneous changes in future ocean biogeochemical variables over marine biota and their broader implications for people. We analyzed modern Earth System Models forced by greenhouse gas concentration pathways until 2100 and showed that the entire world''s ocean surface will be simultaneously impacted by varying intensities of ocean warming, acidification, oxygen depletion, or shortfalls in productivity. In contrast, only a small fraction of the world''s ocean surface, mostly in polar regions, will experience increased oxygenation and productivity, while almost nowhere will there be ocean cooling or pH elevation. We compiled the global distribution of 32 marine habitats and biodiversity hotspots and found that they would all experience simultaneous exposure to changes in multiple biogeochemical variables. This superposition highlights the high risk for synergistic ecosystem responses, the suite of physiological adaptations needed to cope with future climate change, and the potential for reorganization of global biodiversity patterns. If co-occurring biogeochemical changes influence the delivery of ocean goods and services, then they could also have a considerable effect on human welfare. Approximately 470 to 870 million of the poorest people in the world rely heavily on the ocean for food, jobs, and revenues and live in countries that will be most affected by simultaneous changes in ocean biogeochemistry. These results highlight the high risk of degradation of marine ecosystems and associated human hardship expected in a future following current trends in anthropogenic greenhouse gas emissions.     

单细胞原生生物在海洋碳汇研究中的重要性和展望

海洋是地球上最大的碳库,通过对CO~2的固定以及与大气物质和能量的交换,海洋对全球气候的变化起到关键的调控作用。随着全球气候变化的加剧,增加海洋碳汇已经成为应对全球气候变化的热门研究课题和主要途径之一。海洋微型生物在海洋的固碳过程及碳循环中起到关键的作用,对海洋碳汇意义重大。本文综述了一类重要的海洋微型生物——单细胞原生生物在海洋碳汇研究中的重要性,分析了其中的代表——网粘菌门(Labyrintholomycota)原生生物在海洋碳循环和次级生产中的意义,并从清楚地认识海洋碳汇的过程和机制方面,提出未来该领域急需解决的科学问题和可能的研究方案,为丰富海洋碳汇研究的生物学基础提供理论依据。     

Viral attack exacerbates the susceptibility of a bloom‐forming alga to ocean acidification

Both ocean acidification and viral infection bring about changes in marine phytoplankton physiological activities and community composition. However, little information is available on how the relationship between phytoplankton and viruses may be affected by ocean acidification and what impacts this might have on photosynthesis‐driven marine biological CO₂ pump. Here, we show that when the harmful bloom alga Phaeocystis globosa is infected with viruses under future ocean conditions, its photosynthetic performance further decreased and cells became more susceptible to stressful light levels, showing enhanced photoinhibition and reduced carbon fixation, up‐regulation of mitochondrial respiration and decreased virus burst size. Our results indicate that ocean acidification exacerbates the impacts of viral attack on P. globosa, which implies that, while ocean acidification directly influences marine primary producers, it may also affect them indirectly by altering their relationship with viruses. Therefore, viruses as a biotic stressor need to be invoked when considering the overall impacts of climate change on marine productivity and carbon sequestration.     

木质素在海洋中的生物转化及其对海洋碳循环的影响

微型生物参与的海洋碳汇是海洋重要的储碳途径,可调节全球气候变化。木质素是地球上第二大光合而成的碳库,其在海洋中的生物地球化学过程与海洋碳循环密切相关。异养微生物所主导的代谢活动是木质素生物转化的主要途径。近年来,迅速发展的高通量测序技术与传统微生物技术相结合,在探索自然生境中木质素代谢菌群,发现木质素代谢新物种,挖掘相关功能基因等方面已取得一系列成果。然而绝大多数的研究主要集中于陆地生态系统,对于海洋生态系统的研究仍较少。陆源有机碳在海洋中的转化过程仍是一个"谜",故解析海洋木质素碳转化是海洋碳循环研究的重要任务。本文综述了参与海洋木质素转化的功能微生物、木质素代谢机理以及微生物碳代谢活动与海洋碳汇过程的内在联系,为今后的研究提供参考。     

陆地和淡水生态系统新型微生物氮循环研究进展

氮生物地球化学循环是地球物质循环的重要枢纽,是决定陆地生态系统生产力水平、水资源安全、温室气体生成排放的关键过程。氮循环是由微生物介导的一系列复杂过程,不同形态、价态氮化合物的转化分别由相应的功能微生物驱动完成。随着厌氧氨氧化、完全氨氧化等新型氮转化过程的相继报道和发现更新了人们对氮循环的认识。本文综述了陆地和淡水生态系统中厌氧氨氧化(anammox)、硝酸盐异化还原为铵(DNRA)、完全氨氧化(comammox)等新型氮循环过程的发生机制、热区分布及环境效应,并总结了这三种氮循环的相互关系。     

A Synthesis of Climate and Vegetation Cover Effects on Biogeochemical Cycling in Shrub-Dominated Drylands

Semi-arid and arid ecosystems dominated by shrubs (“dry shrublands”) are an important component of the global C cycle, but impacts of climate change and elevated atmospheric CO₂ on biogeochemical cycling in these ecosystems have not been synthetically assessed. This study synthesizes data from manipulative studies and from studies contrasting ecosystem processes in different vegetation microsites (that is, shrub or herbaceous canopy versus intercanopy microsites), to assess how changes in climate and atmospheric CO₂ affect biogeochemical cycles by altering plant and microbial physiology and ecosystem structure. Further, we explore how ecosystem structure impacts on biogeochemical cycles differ across a climate gradient. We found that: (1) our ability to project ecological responses to changes in climate and atmospheric CO₂ is limited by a dearth of manipulative studies, and by a lack of measurements in those studies that can explain biogeochemical changes, (2) changes in ecosystem structure will impact biogeochemical cycling, with decreasing pools and fluxes of C and N if vegetation canopy microsites were to decline, and (3) differences in biogeochemical cycling between microsites are predictable with a simple aridity index (MAP/MAT), where the relative difference in pools and fluxes of C and N between vegetation canopy and intercanopy microsites is positively correlated with aridity. We conclude that if climate change alters ecosystem structure, it will strongly impact biogeochemical cycles, with increasing aridity leading to greater heterogeneity in biogeochemical cycling among microsites. Additional long-term manipulative experiments situated across dry shrublands are required to better predict climate change impacts on biogeochemical cycling in deserts.     

珊瑚礁生态系统病毒研究进展

病毒对珊瑚礁生态系统中的生物进化、生物地球化学循环、珊瑚疾病等方面具有重要的生态影响。随着珊瑚礁的全球性退化,病毒在珊瑚礁生态系统中的功能与危害日益显现。综述了珊瑚礁生态系统中病毒的研究现状与进展,包括：（1）珊瑚礁病毒的多样性与分布特征（水体、宿主、核心病毒组）;（2）珊瑚礁病毒的生态功能（感染方式、促进生物进化、生物地球化学循环）;（3）珊瑚礁病毒对全球气候变化的响应（热压力、珊瑚疾病）。总体而言,珊瑚礁生态系统具有极高的病毒多样性,所发现的60个科占已知所有病毒科数量的58%。珊瑚的核心病毒组主要由双链DNA病毒、单链DNA病毒、单链逆转录病毒所组成,珊瑚黏液层对病毒具有富集作用。"Piggyback-the-Winner"（依附-胜利）是病毒在珊瑚礁中主要的生物动力学模式,其可通过水平基因迁移的方式促进礁区生物进化。病毒可通过裂解细菌与浮游藻类的途径参与珊瑚礁的生物地球化学循环,尤其是碳循环与氮循环过程。此外,病毒还具有介导珊瑚热白化与直接引发珊瑚疾病的能力,这会影响珊瑚礁生态系统应对气候变化的适应性与恢复力。基于国际上的研究进展综述,结合南海珊瑚礁生态现状提出以下研究方向,以期促进我国珊瑚礁病毒学的发展：（1）开展南海珊瑚礁中病毒多样性的识别及其时-空分布特征研究;（2）探索病毒对南海珊瑚热白化、珊瑚疾病的介导作用及其与气候变化的关系;（3）揭示病毒对南海珊瑚礁生物地球化学循环的贡献。     

Winter climate change in plant–soil systems: summary of recent findings and future perspectives

The winter climate is changing in many parts of the world, and it is predicted that winter climate change will modify the structure and function of plant–soil systems. An understanding of these changes and their consequences in terrestrial ecosystems requires knowledge of the linkage between above- and below-ground components as well as the species interactions found in plant–soil systems, which have important implications for biogeochemical cycles. However, winter climate-change studies have focused on only a part of the ecosystem or ecological process. We summarize here recent findings related to the effects of winter climate and its changes on soil nitrogen (N) dynamics, greenhouse gas (N₂O) emissions from the soil, N use by individual plants, vegetation development, and interactions between vegetation and pollinators to generate an integrative understanding of the response of the plant–soil system to winter climate change. This review indicates that the net effects on plants, soil microbes, pollinators, and the associated biogeochemical cycles are balanced among several processes and are highly variable depending on the context, such as the target species/functional group, original winter condition of the habitat, and type of climate change. The consequences of winter climate change for species interactions among plants, associated animals, and biogeochemical cycles are largely unknown. For further research, a large-scale comparative study to measure ecosystem-level functions is important, especially in less-cold ecosystems.     

The impacts of climate change in coastal marine systems

Anthropogenically induced global climate change has profound implications for marine ecosystems and the economic and social systems that depend upon them. The relationship between temperature and individual performance is reasonably well understood, and much climate-related research has focused on potential shifts in distribution and abundance driven directly by temperature. However, recent work has revealed that both abiotic changes and biological responses in the ocean will be substantially more complex. For example, changes in ocean chemistry may be more important than changes in temperature for the performance and survival of many organisms. Ocean circulation, which drives larval transport, will also change, with important consequences for population dynamics. Furthermore, climatic impacts on one or a few 'leverage species' may result in sweeping community-level changes. Finally, synergistic effects between climate and other anthropogenic variables, particularly fishing pressure, will likely exacerbate climate-induced changes. Efforts to manage and conserve living marine systems in the face of climate change will require improvements to the existing predictive framework. Key directions for future research include identifying key demographic transitions that influence population dynamics, predicting changes in the community-level impacts of ecologically dominant species, incorporating populations' ability to evolve (adapt), and understanding the scales over which climate will change and living systems will respond.     

Biogeochemical implications of climate change for tropical rivers and floodplains

Large rivers of the tropics, many of which have extensive floodplains and deltas, are important in the delivery of nutrients and sediments to marine environments, in methane emission to the atmosphere and in providing ecosystem services associated with their high biological productivity. These ecosystem functions entail biogeochemical processes that will be influenced by climate change. Evidence for recent climate-driven changes in tropical rivers exists, but remains equivocal. Model projections suggest substantial future climate-driven changes, but they also underscore the complex interactions that control landscape water balances, river discharges and biogeochemical processes. The most important changes are likely to involve: (1) aquatic thermal regimes, with implications for thermal optima of plants and animals, rates of microbially mediated biogeochemical transformations, density stratification of water bodies and dissolved oxygen depletion; (2) hydrological regimes of discharge and floodplain inundation, which determine the ecological structure and function of rivers and floodplains and the extent and seasonality of aquatic environments; and (3) freshwater–seawater gradients where rivers meet oceans, affecting the distribution of marine, brackish and freshwater environments and the biogeochemical processing as river water approaches the coastal zone. In all cases, climate change affects biogeochemical processes in concert with other drivers such as deforestation and other land use changes, dams and other hydrological alterations and water withdrawals. Furthermore, changes in riverine hydrology and biogeochemistry produce potential feedbacks to climate involving biogeochemical processes such as decomposition and methane emission. Future research should seek improved understanding of these changes, and long-term monitoring should be extended to shallow waters of wetlands and floodplains in addition to the larger lakes and rivers that are most studied.     

Climate change–contaminant interactions in marine food webs: Toward a conceptual framework

Climate change is reshaping the way in which contaminants move through the global environment, in large part by changing the chemistry of the oceans and affecting the physiology, health, and feeding ecology of marine biota. Climate change‐associated impacts on structure and function of marine food webs, with consequent changes in contaminant transport, fate, and effects, are likely to have significant repercussions to those human populations that rely on fisheries resources for food, recreation, or culture. Published studies on climate change–contaminant interactions with a focus on food web bioaccumulation were systematically reviewed to explore how climate change and ocean acidification may impact contaminant levels in marine food webs. We propose here a conceptual framework to illustrate the impacts of climate change on contaminant accumulation in marine food webs, as well as the downstream consequences for ecosystem goods and services. The potential impacts on social and economic security for coastal communities that depend on fisheries for food are discussed. Climate change–contaminant interactions may alter the bioaccumulation of two priority contaminant classes: the fat‐soluble persistent organic pollutants (POPs), such as polychlorinated biphenyls (PCBs), as well as the protein‐binding methylmercury (MeHg). These interactions include phenomena deemed to be either climate change dominant (i.e., climate change leads to an increase in contaminant exposure) or contaminant dominant (i.e., contamination leads to an increase in climate change susceptibility). We illustrate the pathways of climate change–contaminant interactions using case studies in the Northeastern Pacific Ocean. The important role of ecological and food web modeling to inform decision‐making in managing ecological and human health risks of chemical pollutants contamination under climate change is also highlighted. Finally, we identify the need to develop integrated policies that manage the ecological and socioeconomic risk of greenhouse gases and marine pollutants.     

Quantitative estimates of changes in marine and terrestrial primary productivity over the past 300 million years

Changes in marine primary production over geological time have influenced a network of global biogeochemical cycles with corresponding feedbacks on climate. However, these changes continue to remain largely unquantified because of uncertainties in calculating global estimates from sedimentary palaeoproductivity indicators. I therefore describe a new approach to the problem using a mass balance analysis of the stable isotopes (¹⁸O/¹⁶O) of oxygen with modelled O₂ fluxes and isotopic exchanges by terrestrial vegetation for 300, 150, 100 and 50 million years before present, and the treatment of the Earth as a closed system, with respect to the cycling of O₂. Calculated in this way, oceanic net primary productivity was low in the Carboniferous but high (up to four times that of modern oceans) during the Late Jurassic, mid-Cretaceous and early Eocene greenhouse eras with a greater requirement for key nutrients. Such a requirement would be compatible with accelerated rates of continental weathering under the greenhouse conditions of the Mesozoic and early Tertiary. These results indicate possible changes in the strength of a key component of the oceanic carbon (organic and carbonate) pump in the geological past, with a corresponding feedback on atmospheric CO₂ and climate, and provide an improved framework for understanding the role of ocean biota in the evolution of the global biogeochemical cycles of C, N and P.     

Temperature-Induced Viral Resistance in Emiliania huxleyi (Prymnesiophyceae)

Annual Emiliania huxleyi blooms (along with other coccolithophorid species) play important roles in the global carbon and sulfur cycles. E. huxleyi blooms are routinely terminated by large, host-specific dsDNA viruses, (Emiliania huxleyi Viruses; EhVs), making these host-virus interactions a driving force behind their potential impact on global biogeochemical cycles. Given projected increases in sea surface temperature due to climate change, it is imperative to understand the effects of temperature on E. huxleyi’s susceptibility to viral infection and its production of climatically active dimethylated sulfur species (DSS). Here we demonstrate that a 3°C increase in temperature induces EhV-resistant phenotypes in three E. huxleyi strains and that successful virus infection impacts DSS pool sizes. We also examined cellular polar lipids, given their documented roles in regulating host-virus interactions in this system, and propose that alterations to membrane-bound surface receptors are responsible for the observed temperature-induced resistance. Our findings have potential implications for global biogeochemical cycles in a warming climate and for deciphering the particular mechanism(s) by which some E. huxleyi strains exhibit viral resistance.     

Climate change and marine plankton

Understanding how climate change will affect the planet is a key issue worldwide. Questions concerning the pace and impacts of climate change are thus central to many ecological and biogeochemical studies, and addressing the consequences of climate change is now high on the list of priorities for funding agencies. Here, we review the interactions between climate change and plankton communities, focusing on systematic changes in plankton community structure, abundance, distribution and phenology over recent decades. We examine the potential socioeconomic impacts of these plankton changes, such as the effects of bottom-up forcing on commercially exploited fish stocks (i.e. plankton as food for fish). We also consider the crucial roles that plankton might have in dictating the future pace of climate change via feedback mechanisms responding to elevated atmospheric CO(2) levels. An important message emerges from this review: ongoing plankton monitoring programmes worldwide will act as sentinels to identify future changes in marine ecosystems.     

The influence of viral infection on a plankton ecosystem undergoing nutrient enrichment

It is increasingly recognised that viruses are a significant active component of oceanic plankton ecosystems. They play an important role in biogeochemical cycles as well as being implicated in observed patterns of species abundance and diversity. The influence of viral infection in plankton ecosystems is not fully understood. Here we use a number of well-founded mathematical models to investigate the interplay of the ecological and epidemiological interactions of plankton and viruses in the sea. Of particular interest is the role of nutrient on the population dynamics. Nutrient forcing has been suggested as a means of absorbing excess anthropogenic atmospheric carbon dioxide by stimulating increased phytoplankton primary productivity. Here we show that enriching nutrient levels in the sea may decrease the amount of infected phytoplankton species thereby additionally enhancing the efficiency of the biological pump, a means by which carbon is transferred from the atmosphere to the deep ocean.     

A chemical arms race at sea mediates algal host-virus interactions

Despite the critical importance of viruses in shaping marine microbial ecosystems and lubricating upper ocean biogeochemical cycles, relatively little is known about the molecular mechanisms mediating phytoplankton host-virus interactions. Recent work in algal host-virus systems has begun to shed novel insight into the elegant strategies of viral infection and subcellular regulation of cell fate, which not only reveal tantalizing aspects of viral replication and host resistance strategies but also provide new diagnostic tools toward elucidating the impact of virus-mediated processes in the ocean. Widespread lateral gene transfer between viruses and their hosts plays a prominent role in host-virus diversification and in the regulation of host-virus infection mechanisms by allowing viruses to manipulate and 'rewire' host metabolic pathways to facilitate infection.