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: 1754597
• 负责人: Jacob Russell
• 金额: $ 48.76万
• 依托单位: Drexel University
• 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=1754597&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.

昆虫构成了地球上动物多样性的主体，经常被称为“共生体”的微生物感染。微生物共生体可以对它们的宿主昆虫产生很大的影响，塑造它们与其他物种的相互作用或它们对非生命环境的反应。这一点在以植物汁液为食的昆虫中得到了充分的研究，这些昆虫被称为蚜虫，它们可以携带十多种母体转移的共生体物种的各种组合。这些共生体影响蚜虫与食物植物的相互作用，保护蚜虫免受寄生虫和病原体的攻击，或减轻温度变化的影响。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“隐藏参与者”的作用以及共生体功能的潜在机制对于促进人类在作物保护和预防疾病传播方面的利益至关重要。迄今为止，大多数研究都调查了单一共生物种感染的影响，尽管大多数昆虫携带多物种共生“群落”。该奖项将使用具有良好特征的细菌共生体的高度可处理的蚜虫模型系统，以确定多种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，来研究这些效应是如何产生的。由于母体转移的共生体在昆虫中广泛存在，因此蚜虫模型的发现与作物和医疗害虫相关。此外，该奖项还支持高中、本科、研究生和博士后研究人员的培训和专业发展，并包括深入研究人员社区的外展活动。豌豆蚜虫（Acyrthosiphon pisum）拥有多种兼性、母系转移的共生体，是防御性共生的重要模式。最近的实地研究表明，大多数具有兼性共生体的豌豆蚜虫个体都有两个或两个以上的物种。有趣的是，共生体的分布是非随机的，一些共生体对之间的共感染丰富，而另一些共生体对之间的共感染很少，这导致了自然选择倾向于具有不同防御作用的共生体之间的共感染的预测，建立了“多面手”蚜虫，保护它们免受多种威胁。然而，这种伙伴关系中的一小部分可能受到青睐，因为罕见的共生伙伴之间的配对可能会增加成本或突发致病性。另外，一些合并感染的罕见可能源于宿主内部共生相互作用，包括竞争和由此导致的传播率下降。相反，常见的共感染可能源于非竞争的、合作的共生体，它们相互增强了传播。该奖项将通过对工程蚜虫品系的操作实验来测试这些不同的情况，以测量共同感染环境对共生介导的保护性表型和共生转移率的影响。共生体密度和定位将与蚜虫适应性、防御表型、共生体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用于确定竞争和合作动态的潜在机制，预测豌豆蚜虫“共生体”群落的结构。这项研究将加强对害虫多重共生的认识，有助于减轻它们对人类健康、牲畜、农业和基础设施的损害。它将为高中生、本科生、研究生和博士后提供培训，并加强与当地社区的联系。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值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

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.

Context‐dependent vertical transmission shapes strong endosymbiont community structure in the pea aphid, Acyrthosiphon pisum

• DOI: 10.1111/mec.14449
• 发表时间: 2018-04
• 期刊: Molecular Ecology
• 影响因子: 4.9
• 作者: Danielle I Rock;Andrew H. Smith;Jonah Joffe;Amie Albertus;Narayan Wong;Michael O'Connor;K. Oliver;J. Russell

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