Collaborative Research: Competition and cooperation in the defensive symbiont communities of aphids

合作研究：蚜虫防御性共生群落的竞争与合作

• 批准号: 1754302
• 负责人: Kerry Oliver
• 金额: $ 56.92万
• 依托单位: University of Georgia Research Foundation Inc
• 依托单位国家: 美国
• 项目类别: Standard Grant
• 财政年份: 2018
• 资助国家: 美国
• 起止时间: 2018-07-15 至 2023-06-30
• 项目状态: 已结题
• 来源: https://www.nsf.gov/awardsearch/showAward?AWD_ID=1754302&HistoricalAwards=false
• 关键词: Collaborative; Research; Competition; cooperation; defensive

Insects comprise the bulk of animal diversity on the planet and are often infected with microbes called 'symbionts'. Microbial symbionts can have large effects on their host insects, shaping their interactions with other species or their responses to the non-living environment. This is especially well-studied for plant sap-feeding insects, known as aphids, which can carry various combinations of over ten maternally transferred symbiont species. These symbionts influence aphids' interactions with food plants, protect aphids from attack by parasites and pathogens, or alleviate the effects of temperature changes. Since insects are important vectors of human disease and major agricultural pests, understanding the roles of these 'hidden players', and the mechanisms underlying symbiont function is important to further human interests in crop protection and preventing disease spread. Most studies to date have investigated the effects of single symbiont species infections, even though most insects carry multi-species symbiont 'communities'. This award will use a highly-tractable aphid model system, with well-characterized bacterial symbionts, to identify the effects of competition and cooperation amongst multiple symbionts on symbiont transmission, localization and aphid biology. Researchers will use newly developed culturing methods combined with genomic and gene expression studies, to investigate how these effects are generated. Since maternally transferred symbionts are widespread in insects, findings from the aphid model are relevant to crop and medical pests. In addition, this award supports the training and professional development of high school, undergraduate, graduate and post-doctoral researchers, and includes outreach events into the communities of the investigators. The pea aphid, Acyrthosiphon pisum, harbors a diverse cohort of facultative, maternally transferred symbionts and is an important model for defensive symbiosis. Recent field-based research shows that most individual pea aphids, with a facultative symbiont, harbor two or more species. Interestingly, symbiont distributions are non-random, with enriched co-infection among some symbiont pairs and rare co-infection among others, leading to the prediction that natural selection favors co-infections between symbionts with distinct defensive roles, establishing 'generalist' aphids protected against multiple threats. However, just a subset of such partnerships is likely favored as pairings between rare symbiont partners could heighten costs or emergent pathogenicity. Alternatively, rarity of some co-infections may stem from within-host symbiont interactions, including competition and resulting decreases in transmission rates. Conversely, common co-infections may stem from non-competing, cooperative symbionts that reciprocally enhance transmission. This award will test these different scenarios through manipulative experiments on engineered aphid lines that measure the impacts of co-infection context on symbiont-mediated protective phenotypes and rates of symbiont transfer. Symbiont densities and localization will be linked to aphid fitness, defensive phenotypes, symbiont interactions, and rates of transmission. In addition, genomic and gene-expression analyses of symbionts will be used to identify mechanisms underlying competitive and cooperative dynamics that are predicted to structure pea aphids' symbiont 'communities'. This research will enhance the understanding of multipartite symbioses in insect pests, with implications for mitigating their damage to human health, livestock, agriculture, and infrastructure. It will provide training to high school, undergraduate, graduate and postdoctoral students and enhance outreach to the local community.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

昆虫构成了地球上大部分动物的多样性，它们经常被称为共生体的微生物感染。微生物共生体可以对寄主昆虫产生很大影响，塑造它们与其他物种的相互作用或对非生物环境的反应。对于以植物汁液为食的昆虫，也就是所谓的蚜虫来说，这一点尤其得到了充分的研究，这种昆虫可以携带十多种母性转移的共生体的各种组合。这些共生体影响了蚜虫与食用植物的相互作用，保护了蚜虫免受寄生虫和病原体的攻击，或者减轻了温度变化的影响。由于昆虫是人类疾病和主要农业害虫的重要媒介，了解这些隐藏的参与者的作用以及共生功能的潜在机制对于进一步促进人类在作物保护和防止疾病传播方面的利益具有重要意义。到目前为止，大多数研究都调查了单一共生体感染的影响，尽管大多数昆虫携带多个共生体‘群落’。该奖项将使用高度易驯化的蚜虫模型系统，以及具有良好特征的细菌共生体，以确定多个共生体之间的竞争和合作对共生体传播、定位和蚜虫生物学的影响。研究人员将使用新开发的培养方法，结合基因组和基因表达研究，来研究这些影响是如何产生的。由于母性转移的共生体在昆虫中广泛存在，因此来自蚜虫模型的发现与作物和药用害虫有关。此外，该奖项支持高中、本科生、研究生和博士后研究人员的培训和专业发展，并包括进入调查人员社区的外联活动。豌豆蚜(Acyrthosiphon Pisum)具有多种兼性、母性转移的共生体，是防御性共生的重要模式。最近的田间研究表明，大多数豌豆蚜个体具有兼性共生体，拥有两个或两个以上的物种。有趣的是，共生菌的分布是非随机的，一些共生菌对之间存在丰富的共生感染，而另一些共生体对之间的共生感染很罕见，这导致了自然选择有利于具有不同防御作用的共生体之间的共生感染，从而建立了针对多种威胁的“多面手”蚜虫。然而，只有这种伙伴关系的一部分可能受到青睐，因为罕见的共生体伙伴之间的配对可能会增加成本或紧急致病性。或者，一些联合感染的罕见可能源于宿主内部的共生体相互作用，包括竞争和导致传播率下降。相反，常见的联合感染可能源于相互促进传播的非竞争、合作共生体。该奖项将通过在工程化的蚜虫品系上进行操纵性实验来测试这些不同的场景，这些实验测量了共感染环境对共生体介导的保护表型和共生体转移速率的影响。共生菌的密度和定位将与蚜虫的适合度、防御表型、共生菌的相互作用和传播率有关。此外，共生体的基因组和基因表达分析将被用于识别潜在的竞争和合作动态的机制，这些机制被预测为构建豌豆蚜虫的共生体‘群落’。这项研究将加强对害虫中多方共生的理解，并对减轻其对人类健康、牲畜、农业和基础设施的损害具有重要意义。它将为高中、本科生、研究生和博士后学生提供培训，并加强与当地社区的联系。该奖项反映了NSF的法定使命，并通过使用基金会的智力优势和更广泛的影响审查标准进行评估，被认为值得支持。

项目成果

Cryptic community structure and metabolic interactions among the heritable facultative symbionts of the pea aphid

• DOI: 10.1111/jeb.14216
• 发表时间: 2023-09-13
• 期刊: JOURNAL OF EVOLUTIONARY BIOLOGY
• 影响因子: 2.1
• 作者: Peng, Linyao;Hoban, Jessica;Russell, Jacob A.
• 通讯作者: Russell, Jacob A.

Editorial overview: Microbial manipulation of insect-parasite interactions

编辑概述：昆虫与寄生虫相互作用的微生物操纵

• DOI: 10.1016/j.cois.2019.04.005
• 发表时间: 2019
• 期刊: Current opinion in insect science
• 影响因子: 5.3
• 作者: Oliver, KM

Does getting defensive get you anywhere?—Seasonal balancing selection, temperature, and parasitoids shape real‐world, protective endosymbiont dynamics in the pea aphid

• DOI: 10.1111/mec.15906
• 发表时间: 2021-04
• 期刊: Molecular Ecology
• 影响因子: 4.9
• 作者: Andrew H. Smith;M. O’connor;B. Deal;Coleman Kotzer;Amanda Lee;Barrett Wagner;Jonah Joffe

More Is Not Always Better: Coinfections with Defensive Symbionts Generate Highly Variable Outcomes

更多并不总是更好：与防御性共生体的混合感染会产生高度可变的结果

• DOI: 10.1128/aem.02537-19
• 发表时间: 2020
• 期刊: Applied and Environmental Microbiology
• 影响因子: 4.4
• 作者: Weldon, S. R.;Russell, J. A.;Oliver, K. M.;Johnson, Karyn N.
• 通讯作者: Johnson, Karyn N.

Bacteriophage acquisition restores protective mutualism

噬菌体的获得恢复了保护性互利共生

• DOI: 10.1099/mic.0.000816
• 发表时间: 2019
• 期刊: Microbiology
• 影响因子: 1.5
• 作者: Lynn-Bell, Nicole L.;Strand, Michael R.;Oliver, Kerry M.
• 通讯作者: Oliver, Kerry M.