Symbiosis research, technology, and education: Proceedings of the 6th International Symbiosis Society Congress held in Madison Wisconsin, USA, August 2009

Symbiosis, the intimate association between two or more organisms, is a fundamental component of biological systems. Our ability to understand the processes involved in the establishment and function of Symbiosis has critical consequences for the health of humans and the world we live in. For example, a deeper understanding of how legumes and insects have harnessed the nitrogen-fixing capacity of microbes can pave the way toward novel strategies to decrease fertilizer use. Also, using insect models to elucidate links between diet, gut microbiota, and toxin sensitivity not only has implications for biological control strategies, but also will lend insights into similar links in the human gut ecosystem. These types of ideas were presented and discussed at the 6th International Symbiosis Society Congress held in Madison, Wisconsin August, 2009. Over 300 participants from 20 countries attended the 7-day event, which featured cutting-edge symbiosis research from many different perspectives and disciplines. The conference was organized thematically, with oral sessions focused on Evolution, Ecology, Metabolism, the Host-Microbe Interface, Threats to Earth Systems, Symbiosis Models and the Human Microbiome, Viruses and Organelles, and Symbiosis Education. World-renowned scientists, post-doctoral fellows, and students were given the opportunity to describe their most recent discoveries. Session chairs provided overviews of their programs which highlight how the comparative analysis of different systems reveal common trends underlying symbiotic associations, what tools and theory are being developed that may be applied more broadly in symbiosis research, how symbiosis research contributing solutions to global issues such as emerging antibiotic resistance, a need for alternative energy sources, the pursuit of sustainable agriculture and natural resources, and how symbiotic systems are ideal for educating people about the fascinating natural world around us. The following paragraphs provide an overview of the research and discussions that took place during the congress.     

从细胞内共生到多尺度共生：回顾与展望

基于共生概念的历史变化,目前人们普遍接受了广义共生概念。即共生是包含互利共生（mutualism）、偏利共生（commensalism）和拮抗/寄生（antagonism/parasitism）的共生连续体。本文简述了近20年间,全球9次国际共生学术大会取得的重要成果,对细胞内共生、时间、空间以及多种互作尺度共生关系的研究利用进展进行了评述。同时展望了一些活跃共生领域的研究概况,如共生失调 （dysbiosis）、植物-微生物-昆虫三角共生关系（plant-microbe-insect triangle）、细菌-真菌互作（bacterial- fungal interaction,BFI）、菌根菌-真菌内生细菌-植物多方共生联盟（multipartite symbiosis consortium）以及与共生相关微生物组的集合群落（metacommunity）研究及应用等。共生（symbiosis）正成为当代生物学的核心原则,正以一种与更宏大系统方法相一致的概念,从根本上改变了传统上的一些生物学概念,如孤立性的个体（individuality）概念。基因组测序和高通量RNA技术分析揭示,动、植物与共生微生物的重要互作,打破了迄今为止生物个体的特征边界,挑战了这些学科的定义;共生不仅是一对一的互利共生关系,共生实际是多种共生模式的连续共生体。此外,植物-昆虫-微生物互作的三角关系;菌根-真菌-真菌内生细菌-植物的多方联盟等新关系的发现,更把生命科学推向了快速发展的方向。这些科学进展不仅对生物科学的遗传学、免疫学、进化、发育、解剖学和生理学的研究至关重要,拓宽了新的视野,而且对农业中生物制剂研发,人类微生物组的管理及调控,以及对发酵食品及工业微生物生产的设计和管理将产生积极影响。     

共生概念发展的历史,现状及展望

本文从回顾历史出发,勾划出国际上极为热门的共生学说发展轨迹,指出共生是一切群体中密切联合的能力,不但是诸多生命分支科学的理论网络,涉及到许多应用问题,而且是一种生物哲学,自然界和人文科学莫不如此。     

Consequences of grazing on the vertical transmission of a fungal Neotyphodium symbiont in an annual grass population

Symbiosis between cool‐season grasses and vertically transmitted fungal endophytes are common and significantly impact on ecosystem function. This makes the understanding of the underlying mechanisms to symbiotic individuals frequency in local populations much more interesting. Most studies have been focused on the differential fitness between symbiotic and non‐symbiotic counterparts (relative fitness), barely considering other mechanisms. We performed a microcosms experiment to evaluate whether grazing alters the dynamics of the endophyte Neotyphodium occultans in the annual grass Lolium multiflorum by simultaneously modifying the relative fitness and the endophyte efficiency to be transmitted from host plants to seeds. Grazing was simulated by means of clipping and trampling on symbiotic and non‐symbiotic plants growing separately, in soils obtained from paddocks, differing in their agronomic management history (natural grassland vs. ryegrass promotion). Seed production showed a complex pattern as it depended on the symbiotic status of the plants, the level of grazing and the agro‐ecological context. Grazed plants produced three times fewer seeds than ungrazed plants only in microcosms with endophyte‐symbiotic plants in soils from ryegrass promotion. Endophyte benefits on seed production were exclusively observed in ungrazed plants in the same soil. Symbiotic plants produced symbiotic and non‐symbiotic seeds in all the treatments. While the production of non‐symbiotic seeds by these plants was not affected by grazing and the soil, grazing reduced the production of symbiotic seeds in both contexts. Grazing negative effect on the density of fully infected spikes determined a significant increment in the transmission failures which were not modified by agro‐ecological contexts. Therefore, grazing can modulate symbiosis dynamics through reducing seed production and endophyte transmission efficiency. Transmission has been disregarded, but it is a context‐dependent process that could lead to a gradual reduction in the symbiotic plants frequency in a population if the mutualism effectiveness does not outweigh transmission failures.     

Growth of Trifolium subterraneum L. Selected for Sparse and Abundant Nodulation as Affected by Root Temperature and Rhizobium Strain

Root temperature greatly affected plant growth whether or notplants depended on symbiotic nitrogen fixation. The two plantselections responded differently to the three strains of Rhizobiumand this response was differentially affected by root temperature. Plant yield was significantly decreased by each fall of 4 °Cin temperature from 19 to 7 °C by amounts that dependedboth on the host and Rhizobium strain. Symbiosis with strainTA1, originally isolated from a cold environment, was most tolerantof a root temperature of 11 °C; TA1 produced as much ormore plant material of the abundantly nodulating host in 40days growth at 7 and 11 °C as did the uninoculated plantsgiven KNO³. Root temperature affected the number, rate of formation, anddistribution of nodules on the root system. At 7 °C fewernodules formed than between 11 and 19 °C. At 7 °C nodulesdid not form on secondary roots by 40 days but at 11 °Cthe secondary roots nodulated rapidly between 30 and 40 days.Nodule formation at 19 °C was almost completed at 20 days,when secondary root nodules accounted for 60 per cent of thetotal. Within the range 15 to 19 °C, at which the originalselections for sparse and abundant nodulation were made, plantsnodulated true to selection, but not at 11 °C. At 7 and11 °C plants nodulated with TA1 yielded more with increasingnumber of nodules.     

Genetic-evolutionary basis of symbiosis doctrine

The author presents the current notion of symbiosis as one of the main adaptation of an organism to changeable environment. Symbiosis is considered as a super organism genetic system within which there are different interactions (including mutualism and antagonism). Genetic integration of symbiotic partners can be realized as cross regulation of their genes, exchange of gene products (proteins, RNA), gene amplification and sometimes gene transfer between organisms. On the phenotypic level these processes result in signal interactions, integration of partner metabolic systems and development of symbiotic organs. Co-evolution is considered as an assemblage of micro- and macroevolution processes basing on pre-adaptations and proceeding under influence of different forms of natural selection (individual, frequency-depended and kin selection). Symbiosis can be compared with sexual process since both are the forms of organism integration characterized by different genetic mechanisms and evolutionary consequences. The genome evolution in symbiotic microorganisms can proceed by: 1) simplification of genome in obligate symbiosis (loss of genes that are necessary for independent existence, transfer of some genes to the host organism); 2) complication of genome in facultative symbiosis (increase in genome plasticity, structural and functional differentiation of genome into systems controlling free-living and symbiotic parts of life cycle). Most of symbiotic interactions are correlated to an increase in genetic plasticity of an organism that can lead to evolutionary saltations and origin of new forms of life.     

Symbiosis of cornulitids with the cystoporate bryozoan Fistulipora in the Pridoli of Saaremaa,Estonia

Cornulites sp. and Fistulipora przhidolensis formed a symbiotic association in the Pridoli (latest Silurian) of Saaremaa Island, Estonia. This Cornulites sp.–F. przhidolensis association is the youngest example of cornulitid–bryozoan symbiosis. Symbiosis is indicated by intergrowth of both organisms. The cornulitids are completely embedded within the cystoporate bryozoan colony, leaving only their apertures free on the growth surface of bryozoan. In terms of food competition, this association could have been slightly harmful to F. przhidolensis as Cornulites sp. may have been a kleptoparasite. There may have been a small escalation in the evolution of the endobiotic life mode of cornulitids as the number of such associations increased from the Ordovician to Silurian. It is likely that Palaeozoic bryozoan symbiosis reached its maximum in the Late Ordovician. Most of the symbiotic bryozoans in the Palaeozoic are trepostomes, and the diversity of symbiotic associations was also greatest among trepostomes.     

Symbiosis specificity in the legume: rhizobial mutualism

Legume plants are able to engage in root nodule symbiosis with nitrogen-fixing soil bacteria, collectively called rhizobia. This mutualistic association is highly specific, such that each rhizobial species/strain interacts with only a specific group of legumes, and vice versa. Symbiosis specificity can occur at multiple phases of the interaction, ranging from initial bacterial attachment and infection to late nodule development associated with nitrogen fixation. Genetic control of symbiosis specificity is complex, involving fine-tuned signal communication between the symbiotic partners. Here we review our current understanding of the mechanisms used by the host and bacteria to choose their symbiotic partners, with a special focus on the role that the host immunity plays in controlling the specificity of the legume - rhizobial symbiosis.     

共生理论视角下创新农业生态经济研究范式

共生理论认为异质共生生物在其生存过程中会表现出相互依存的关系。试图将这一论点移植到农业生态经济研究中,用以处理农业生产中生态效益与经济效益之间矛盾的问题。为此,把农业生态经济视为由生态单元与经济单元组成的异质共生体,分析了该共生体的结构与共生模式,并采用Logistic方程与数值模拟方法,探讨农业生态经济共生体的共生机制,揭示共生单元间的演化规律与成长特征。研究表明:共生模式在农业实践上创新应用的主要目标是将共生体从寄生共生模式向互惠共生模式转型,并提出正向转型的激励策略。共生单元的选择必须具有兼容性,共生单元间有明确的共生界面,促使物质、能量和信息的交流,以增加共生体内自由能。共生关系正向发展要遵循共生演进规律,偏利共生模式是演进到互惠共生模式的必经过程。培育互惠共生适存的共生环境对促进共生体演进至关重要。这些研究成果为农业生态经济研究提供一个新范式,并开创一条研究新思路与方法。     

Symbiotic interactions in the Silurian of Baltica

Thirteen symbiotic associations occur in the Silurian of Baltica. Symbiosis was especially prominent among colonial animals, most commonly with stromatoporoids. These sponges hosted the most diverse fauna of endobiotic symbionts (including rugosans, Syringopora, ‘polychaetes’, cornulitids and lingulids). This pattern can be explained by the abundance of stromatoporoids in the Silurian of Baltica and their large skeletal volume, making them attractive hosts for smaller invertebrates. There is an evolutionary trend of an increasing number of different pairs of symbiotic taxa from the Llandovery to the Ludlow, with a remarkable increase in the Ludlow. This is likely related to an increase in the number of mutualistic taxa that could have had evolutionary advantages over organisms less amenable to symbiosis. The number of different pairs of symbiotic taxa also increased in the Wenlock, which may be linked to delayed recovery from the end‐Ordovician mass extinction.     

Vascular architecture in the bacteriogenic light organ of Euprymna tasmanica (Cephalopoda: Sepiolidae)

Symbiosis between southern dumpling squid, Euprymna tasmanica (Cephalopoda: Sepiolidae), and its luminescent symbiont, the bacterium Vibrio fischeri, provides an experimentally tractable system to examine interactions between the eukaryotic host and its bacterial partner. Luminescence emitted by the symbiotic bacteria provides light for the squid in a behavior termed “counter‐illumination,” which allows the squid to mask its shadow amidst downwelling moonlight. Although this association is beneficial, light generated from the bacteria requires large quantities of oxygen to maintain this energy‐consuming reaction. Therefore, we examined the vascular network within the light organ of juveniles of E. tasmanica with and without V. fischeri. Vessel type, diameter, and location of vessels were measured. Although differences between symbiotic and aposymbiotic squid demonstrated that the presence of V. fischeri does not significantly influence the extent of vascular branching at early stages of symbiotic development, these finding do provide an atlas of blood vessel distribution in the organ. Thus, these results provide a framework to understand how beneficial bacteria influence the development of a eukaryotic closed vascular network and provide insight to the evolutionary developmental dynamics that form during mutualistic interactions.     

根瘤菌共生固氮能力的进化模式

根瘤菌-豆科植物共生固氮体系对农业的可持续性发展至关重要,也是研究原核与真核生物互利共生的模式体系之一。长期以来,根瘤菌共生固氮相关研究主要集中在结瘤因子与固氮酶合成及调控等少数关键基因,但仅获得这些关键基因却不能保证细菌获得结瘤固氮能力。随着比较和功能基因组学的快速发展和应用,越来越多的研究发现根瘤菌使用了很多系统发育分支特异的遗传机制与豆科植物建立有效的共生关系,进一步揭示了双方互利共生的复杂性。本综述总结了近年来比较基因组学、遗传学以及实验进化等方面的相关研究进展,在此基础上讨论根瘤菌共生固氮能力的进化模式。     

网络分析在宿主植物与菌根真菌共生关系研究中的应用

菌根共生体是生物界最广泛的互惠共生体,共生关系多样性是生物多样性的重要组成部分,当前群落尺度菌根共生关系研究才刚刚起步,但发展迅速。网络分析作为生态学研究的重要手段逐渐在菌根共生关系中得以应用,网络分析为群落尺度探究菌根真菌多样性分布规律、共生机制研究提供新观点和途径,对菌根真菌群落结构、生态功能研究具有重要意义。本文总结了网络分析方法在单点式、双点式和多点式菌根共生关系网络研究中的优势和局限性,同时还阐述了零模型选择和构建网络大小对关系网络度量指数的影响,为菌根真菌群落结构、生态功能研究提供新思路,为后续群落尺度菌根共生关系格局研究提供借鉴。     

Stress at the Korean Mountains: meeting report of the 8th International Workshop on the Molecular Biology of Stress Responses

South Korea is a country exemplified by a combination of upscale new technology and ancient mysticism. The busy streets of Seoul hustle and bustle like any large, active metropolis, yet the city's inhabitants radiate an intrinsic sense of peace, creating a timeless atmosphere. The combination of emerging technology and profound respect for the Korean culture and heritage makes this country a unique environment in which to organize a successful scientific meeting. Cell Stress Society International, in its quest to cross the cultural frontiers of science and propagate research on the stress response, partnered with the newly created Korean Cell Stress Society to hold the 8th International Workshop on the Molecular Biology of Stress Responses on June 1–4, 2010.     

Evaluation of the FORAM index in a case of conservation

Localized and global impacts are responsible for driving the current decline in coral reef ecosystems. The worldwide debate over the efficacy of Marine Protected Areas (MPAs) as a conservation measure for coral reefs highlights the importance of acquiring accurate indicators of reef resilience and recovery under stressful conditions. Marine benthic foraminifera, considered outstanding indicators for environmental changes, are unicellular eukaryotes that inhabit sandy sediments in coral reefs. There are three kinds of benthic foraminifera: symbiotic, opportunistic, and other small heterotrophic. Symbiosis with microalgae is not favorable under high nutrient conditions. This study compared the FORAM Index (FI) in different sites inside and outside MPAs. The index was also compared with coral and algae cover. High FI values are characteristic of healthy oligotrophic reefs whereas low values represent eutrophicated ecosystems. A community structure analysis was done in order to determine the compositional change of functional groups, and thus, to test spatially the index efficiency and performance. In general, MPA sites presented lower indexes compared to Non-MPA sites, probably due to the higher impact of tourism and agriculture in these areas. On the other hand, the index was not correlated with coral nor algae cover, even though positive and negative trends were found. Assemblage analyzes corroborated that the symbiotic foraminifers’ high susceptibility is the main source for the index variation, which was independent of the substrate type from which it was sampled. Our results show both the efficiency of this index and the importance of its application for evaluating conservation strategies.     

Simulation of evolution implemented in the mutualistic symbioses towards enhancing their ecological efficiency,functional integrity and genotypic specificity

We created the mathematical model for the evolution of the Efficiency of Mutualistic Symbioses (EMS) which was estimated as the microsymbiont impacts on the host’s reproductive potential. Using the example of rhizobia–legume interaction, the relationships were studied between EMS and Functional Integrity of Symbiosis (FIS) which is represented as a measure for concordance of changes in the partners’ genotypic frequencies under the environmental fluctuations represented by the minor deviations of the systemic model parameters. The FIS indices correlate positively with EMS values suggesting an enhancement of FIS via the natural selection operating in the partners’ populations in favor of high EMS. Due to this selection, nodular habitats may be closed for colonization by the non-beneficial bacterial strains and the Genotypic Specificity of Mutualism (GSM) in partners’ interactions is enhanced: the selective advantage of host-specific vs non-host-specific mutualists is increasing. The novelty of our model is to suggest a selective background for macroevolutionary events reorganizing the structure and functions of symbiotic systems and to present its evolution as a result of shifting the equilibrium between different types of mutualists under the impacts of the symbiosis-stipulated modes of natural selection.     

Enigmatic dual symbiosis in the excretory organ of Nautilus macromphalus (Cephalopoda: Nautiloidea)

Symbiosis is an important driving force in metazoan evolution and the study of ancient lineages can provide an insight into the influence of symbiotic associations on morphological and physiological adaptations. In the 'living fossil' Nautilus, bacterial associations are found in the highly specialized pericardial appendage. This organ is responsible for most of the excretory processes (ultrafiltration, reabsorption and secretion) and secretes an acidic ammonia-rich excretory fluid. In this study, we show that Nautilus macromphalus pericardial appendages harbour a high density of a beta-proteobacterium and a coccoid spirochaete using transmission electron microscopy, comparative 16S rRNA sequence analysis and fluorescence in situ hybridization (FISH). These two bacterial phylotypes are phylogenetically distant from any known bacteria, with ammonia-oxidizing bacteria as the closest relatives of the beta-proteobacterium (above or equal to 87.5% sequence similarity) and marine Spirochaeta species as the closest relatives of the spirochaete (above or equal to 89.8% sequence similarity), and appear to be specific to Nautilus. FISH analyses showed that the symbionts occur in the baso-medial region of the pericardial villi where ultrafiltration and reabsorption processes take place, suggesting a symbiotic contribution to the excretory metabolism.     

Edmund Vincent Cowdry and the Making of Gerontology as a Multidisciplinary Scientific Field in the United States

The Canadian–American biologist Edmund Vincent Cowdry played an important role in the birth and development of the science of aging, gerontology. In particular, he contributed to the growth of gerontology as a multidisciplinary scientific field in the United States during the 1930s and 1940s. With the support of the Josiah Macy, Jr. Foundation, he organized the first scientific conference on aging at Woods Hole, Massachusetts, where scientists from various fields gathered to discuss aging as a scientific research topic. He also edited Problems of Ageing (1939), the first handbook on the current state of aging research, to which specialists from diverse disciplines contributed. The authors of this book eventually formed the Gerontological Society in 1945 as a multidisciplinary scientific organization, and some of its members, under Cowdry’s leadership, formed the International Association of Gerontology in 1950. This article historically traces this development by focusing on Cowdry’s ideas and activities. I argue that the social and economic turmoil during the Great Depression along with Cowdry’s training and experience as a biologist – cytologist in particular – and as a textbook editor became an important basis of his efforts to construct gerontology in this direction.     

The International Society of Photosynthesis Research (ISPR) and its associated International Congress on Photosynthesis (ICP): a pictorial report

We present here some thoughts on the origin of the International Society of Photosynthesis Research (ISPR). We provide two tables, one of the Officers of the ISPR and the International Photosynthesis Committee, and the other of the Organizers of the International Congress of Photosynthesis (ICP) from the 14th ICP (PS07 in Glasgow) to the 9th ICP (in Nagoya). In celebration of the 14th ICP, we provide here a collection of photographs of the many involved in the ISPR and the ICP as well as some of the others. We end this presentation with the list of members of the committees of the ISPR. If there are any errors in this report, we request the readers to send them to one of us (G; gov@uiuc.edu). Further, we are seeking recollections on ISPR and the Congresses from all the readers of the events during the 1992–1998 period. Hopefully, these will shed further light on the origin and the evolution of the ISPR. These will aid in the preparation of a more complete history of the origin and the evolution of ISPR for publication in 2008.     

Simulation of evolution implemented in the mutualistic symbioses towards enhancing their ecological efficiency, functional integrity and genotypic specificity

We created the mathematical model for the evolution of the Efficiency of Mutualistic Symbioses (EMS) which was estimated as the microsymbiont impacts on the host’s reproductive potential. Using the example of rhizobia–legume interaction, the relationships were studied between EMS and Functional Integrity of Symbiosis (FIS) which is represented as a measure for concordance of changes in the partners’ genotypic frequencies under the environmental fluctuations represented by the minor deviations of the systemic model parameters. The FIS indices correlate positively with EMS values suggesting an enhancement of FIS via the natural selection operating in the partners’ populations in favor of high EMS. Due to this selection, nodular habitats may be closed for colonization by the non-beneficial bacterial strains and the Genotypic Specificity of Mutualism (GSM) in partners’ interactions is enhanced: the selective advantage of host-specific vs non-host-specific mutualists is increasing. The novelty of our model is to suggest a selective background for macroevolutionary events reorganizing the structure and functions of symbiotic systems and to present its evolution as a result of shifting the equilibrium between different types of mutualists under the impacts of the symbiosis-stipulated modes of natural selection.