Conspecific coprophagy stimulates normal development in a germ-free model invertebrate

Jahnes, Benjamin C.; Herrmann, Madeline; Sabree, Zakee L.

doi:10.7717/peerj.6914

Cited by 33 publications

(31 citation statements)

References 68 publications

(84 reference statements)

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“…Indeed, in order to transmit bacteria from parents to offspring, stinkbugs can attach special symbiont capsules to their eggs (Fukatsu & Hosokawa 2002) or cover eggs with symbiont-supplemented jelly (Kaiwa et al 2014). Feces consumption (cophrophagy) is an important mechanism by which early-stage cockroaches acquire their gut bacteria, increasing their fitness compared to when reared under sterile conditions (Jahnes et al 2019). In dung beetles, vertical transmission is ensured through a brood ball, which results in remarkably faithful microbial transmission (Estes et al 2013).…”

Section: Introductionmentioning

confidence: 99%

When the microbiome defines the host phenotype: selection on vertical transmission in varying environments

Bruijning

Henry

Forsberg

et al. 2020

Preprint

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The microbiome can contribute to variation in fitness-related traits of their hosts, and thus to host evolution. Hosts are therefore expected to be under selection to control their microbiome, for instance through controlling microbe transmission from parents to offspring. Current models have mostly focused on microbes that either increase or decrease fitness. In that case, host-level selection is relatively straightforward, favouring either complete or no inheritance. In natural systems, however, vertical transmission fidelity varies widely, and microbiome composition is often shaped by a combination of vertical and horizontal transmission modes. We propose that such mixed transmission could optimize host fitness under fluctuating environments. Using a general model, we illustrate that decreasing vertical transmission fidelity increases the amount of microbiome variation, and thus potentially phenotypic variation, across hosts. Whether or not this is advantageous depends on environmental conditions, how much the microbiome changes during host development, and the contribution of other factors to trait variation. We discuss how environmentally-dependent microbial effects can favor intermediate transmission, review examples from natural systems, and suggest research avenues to empirically test our predictions. Overall, we show that imperfect transmission may be adaptive by allowing individuals to ensure phenotypic variability in their offspring in contexts where varying environments mean that this strategy increases long-term fitness.

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Section: Introductionmentioning

confidence: 99%

When the microbiome defines the host phenotype: selection on vertical transmission in varying environments

Bruijning

Henry

Forsberg

et al. 2020

Preprint

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“…Interestingly, communities from the colon and stomach, although being the most distal communities characterized here, displayed a high degree of structural and functional similarity. This supported the murine practice of coprophagy where material released from the colon get re-ingested as a way to retain bacterial proteins 43 , to further process some partially digested material 44 , and to re-colonize the GIT 45,46 .…”

Section: Table (Rat)mentioning

confidence: 59%

MetaGeneHunt for protein domain annotation in short-read metagenomes

Berlemont

Winans

Talamantes

et al. 2020

Sci Rep

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the annotation of short-reads metagenomes is an essential process to understand the functional potential of sequenced microbial communities. Annotation techniques based solely on the identification of local matches tend to confound local sequence similarity and overall protein homology and thus don't mirror the complex multidomain architecture and the shuffling of functional domains in many protein families. Here, we present MetaGeneHunt to identify specific protein domains and to normalize the hit-counts based on the domain length. We used MetaGeneHunt to investigate the potential for carbohydrate processing in the mouse gastrointestinal tract. We sampled, sequenced, and analyzed the microbial communities associated with the bolus in the stomach, intestine, cecum, and colon of five captive mice. Focusing on Glycoside Hydrolases (GHs) we found that, across samples, 58.3% of the 4,726,023 short-read sequences matching with a GH domain-containing protein were located outside the domain of interest. next, before comparing the samples, the counts of localized hits matching the domains of interest were normalized to account for the corresponding domain length. Microbial communities in the intestine and cecum displayed characteristic GH profiles matching distinct microbial assemblages. Conversely, the stomach and colon were associated with structurally and functionally more diverse and variable microbial communities. Across samples, despite fluctuations, changes in the functional potential for carbohydrate processing correlated with changes in community composition. Overall MetaGeneHunt is a new way to quickly and precisely identify discrete protein domains in sequenced metagenomes processed with MG-RASt. in addition, using the sister program "GeneHunt" to create custom Reference Annotation Table, MetaGeneHunt provides an unprecedented way to (re)investigate the precise distribution of any protein domain in short-reads metagenomes.

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“…Bacteria in cockroach guts display tremendous phylogenetic diversity, and include members of Bacteroidetes, Firmicutes, Fibrobacteres, and Proteobacteria (Dietrich et al, 2014;Mikaelyan et al, 2015b). The assemblage is dominated by obligate anaerobes, including those that break down structural polysaccharides of plant-based detritus (Bignell, 1977;Cruden and Markovetz, 1979, 1984, produce semiochemicals that influence host social behavior (Wada-Katsumata et al, 2015) and directly affect development by regulating gene expression in their host (Cruden and Markovetz, 1987;Jahnes et al, 2019). Another advantage of trophallaxis is that metabolic products of the parents and their resident microbial assemblage would not be compromised by exposure to the outside environment; these include hormones, enzymes, metabolites, and other chemicals that may serve as physiological or behavioral signals.…”

Section: Host Fitness Benefitsmentioning

confidence: 99%

Origin of Mutualism Between Termites and Flagellated Gut Protists: Transition From Horizontal to Vertical Transmission

Nalepa

2020

Front. Ecol. Evol.

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Lower termites, as well as their sister group, the subsocial wood-feeding cockroach Cryptocercus, rely on flagellated eukaryotic symbionts in the hindgut to cooperatively digest their wood diet. In Cryptocercus these flagellates undergo encystment cycles tightly coordinated with the molting cycle of their host, yet the resultant cysts play no demonstrated role in their transmission to neonates; the trophozoite stage of the flagellates is passed directly from parents to offspring via hindgut fluids (proctodeal trophallaxis). This pattern suggests that encystment is a vestige from a gregarious cockroach ancestor, when the flagellates had a functional, two-stage life cycle and the cysts were horizontally transmitted among hosts via coprophagy. The strong integration between flagellate encystment cycles and host developmental physiology in Cryptocercus indicates that the relationship of the flagellates with their proposed gregarious cockroach ancestor was not commensal, but parasitic, with flagellates likely obtaining benefits by taking advantage of host gut metabolites and ingested plant debris. When vertical transmission evolved the parasites were 'captured,' and their fitness became inescapably embedded in the fitness of their host. The vertical transmission of gut flagellates and the origin of host subsociality via proctodeal trophallaxis can be considered two sides of the same coin. From the host point of view proctodeal trophallaxis marks the origination of parental care by provisioning neonates with nourishment, metabolites and beneficial microbiota. From the flagellate point of view, proctodeal trophallaxis was a shift from horizontal to vertical transmission, pushing them from the parasitic to the mutualistic end of the symbiotic spectrum, arguably making this host behavioral change the most critical juncture in the evolutionary trajectory of the termite lineage.

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Conspecific coprophagy stimulates normal development in a germ-free model invertebrate

Cited by 33 publications

References 68 publications

When the microbiome defines the host phenotype: selection on vertical transmission in varying environments

When the microbiome defines the host phenotype: selection on vertical transmission in varying environments

MetaGeneHunt for protein domain annotation in short-read metagenomes

Origin of Mutualism Between Termites and Flagellated Gut Protists: Transition From Horizontal to Vertical Transmission

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