Happens in the best of subfamilies: establishment and repeated replacements of co‐obligate secondary endosymbionts within Lachninae aphids

Manzano-Marı́n, Alejandro; Szabó, Gitta; Simon, Jean‐Christophe; Horn, Matthias; Latorre, Amparo

doi:10.1111/1462-2920.13633

Cited by 77 publications

(83 citation statements)

References 57 publications

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“…Microbes can also facilitate the establishment of other microbial species within the microbiome community. Some symbiont species are more likely to occur in coinfections; for example, Fukatsui symbiotica (Manzano-Marín, Szabó, Simon, Horn, & Latorre, 2017) is a facultative symbiont that is almost always found in coinfection with…”

Section: Interactions Within Microbial Communitiesmentioning

confidence: 99%

Metacommunity theory for transmission of heritable symbionts within insect communities

Brown

Mihaljevic

Marteaux

et al. 2019

Ecology and Evolution

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Microbial organisms are ubiquitous in nature and often form communities closely associated with their host, referred to as the microbiome. The microbiome has strong influence on species interactions, but microbiome studies rarely take interactions between hosts into account, and network interaction studies rarely consider microbiomes. Here, we propose to use metacommunity theory as a framework to unify research on microbiomes and host communities by considering host insects and their microbes as discretely defined “communities of communities” linked by dispersal (transmission) through biotic interactions. We provide an overview of the effects of heritable symbiotic bacteria on their insect hosts and how those effects subsequently influence host interactions, thereby altering the host community. We suggest multiple scenarios for integrating the microbiome into metacommunity ecology and demonstrate ways in which to employ and parameterize models of symbiont transmission to quantitatively assess metacommunity processes in host‐associated microbial systems. Successfully incorporating microbiota into community‐level studies is a crucial step for understanding the importance of the microbiome to host species and their interactions.

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Section: Interactions Within Microbial Communitiesmentioning

confidence: 99%

Metacommunity theory for transmission of heritable symbionts within insect communities

Brown

Mihaljevic

Marteaux

et al. 2019

Ecology and Evolution

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“…Many of these symbioses display high partner fidelity over long periods of evolutionary time, often with strict co-diversification of host and symbiont lineages [5,6]. However, both symbiont loss and symbiont switching, often to a phylogenetically distant microbial taxon, has been identified in many host lineages, especially among insects [7][8][9][10], as well as in other invertebrate taxa [11]. It has been suggested that symbiont switching may be linked to changes in host traits, e.g.…”

Section: Introductionmentioning

confidence: 99%

Match and mismatch between dietary switches and microbial partners in plant sap-feeding insects

2019

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Some animal groups associate with the same vertically transmitted microbial symbionts over extended periods of evolutionary time, punctuated by occasional symbiont switches to different microbial taxa. Here we test the oft-repeated suggestion that symbiont switches are linked with host diet changes, focusing on hemipteran insects of the suborder Auchenorrhyncha. These insects include the only animals that feed on plant xylem sap through the life cycle, as well as taxa that feed on phloem sap and plant parenchyma cells. Ancestral state reconstruction provides strong statistical support for a xylem feeding auchenorrhynchan ancestor bearing the dual symbiosis with the primary symbiont Sulcia (Bacteroidetes) and companion symbiont 'b-Sym' (b-proteobacteria). We identified seven dietary transitions from xylem feeding (six to phloem feeding, one to parenchyma feeding), but no reversions to xylem feeding; five evolutionary losses of Sulcia, including replacements by yeast symbionts, exclusively in phloem/parenchymafeeding lineages; and 14 -15 losses of b-Sym, including nine transitions to a different bacterial companion symbiont. Our analysis indicates that, although companion symbiont switching is not associated with shifts in host diet, Sulcia is probably required for xylem-feeding. Furthermore, the ancestral auchenorrhynchan bearing Sulcia and b-Sym probably represents the sole evolutionary origin of xylem feeding in the animal kingdom.

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“…2011; Manzano-Marín and Latorre 2014; Manzano-Marín et al. 2016, 2017). Accordingly, Cinara species (Aphididae: Lachninae) have been consistently found to host an additional bacterial co-obligate symbiont, most commonly S. symbiotica (Lamelas et al.…”

Section: Introductionmentioning

confidence: 99%

A Freeloader? The Highly Eroded Yet Large Genome of the Serratia symbiotica Symbiont of Cinara strobi

Manzano-Marı́n

d’Acier

Clamens

et al. 2018

Genome Biology and Evolution

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Genome reduction is pervasive among maternally inherited bacterial endosymbionts. This genome reduction can eventually lead to serious deterioration of essential metabolic pathways, thus rendering an obligate endosymbiont unable to provide essential nutrients to its host. This loss of essential pathways can lead to either symbiont complementation (sharing of the nutrient production with a novel co-obligate symbiont) or symbiont replacement (complete takeover of nutrient production by the novel symbiont). However, the process by which these two evolutionary events happen remains somewhat enigmatic by the lack of examples of intermediate stages of this process. Cinara aphids (Hemiptera: Aphididae) typically harbor two obligate bacterial symbionts: Buchnera and Serratia symbiotica. However, the latter has been replaced by different bacterial taxa in specific lineages, and thus species within this aphid lineage could provide important clues into the process of symbiont replacement. In the present study, using 16S rRNA high-throughput amplicon sequencing, we determined that the aphid Cinara strobi harbors not two, but three fixed bacterial symbionts: Buchnera aphidicola, a Sodalis sp., and S. symbiotica. Through genome assembly and genome-based metabolic inference, we have found that only the first two symbionts (Buchnera and Sodalis) actually contribute to the hosts’ supply of essential nutrients while S. symbiotica has become unable to contribute towards this task. We found that S. symbiotica has a rather large and highly eroded genome which codes only for a few proteins and displays extensive pseudogenization. Thus, we propose an ongoing symbiont replacement within C. strobi, in which a once “competent” S. symbiotica does no longer contribute towards the beneficial association. These results suggest that in dual symbiotic systems, when a substitute cosymbiont is available, genome deterioration can precede genome reduction and a symbiont can be maintained despite the apparent lack of benefit to its host.

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Happens in the best of subfamilies: establishment and repeated replacements of co‐obligate secondary endosymbionts within Lachninae aphids

Cited by 77 publications

References 57 publications

Metacommunity theory for transmission of heritable symbionts within insect communities

Metacommunity theory for transmission of heritable symbionts within insect communities

Match and mismatch between dietary switches and microbial partners in plant sap-feeding insects

A Freeloader? The Highly Eroded Yet Large Genome of the Serratia symbiotica Symbiont of Cinara strobi

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