Currency, Exchange, and Inheritance in the Evolution of Symbiosis

Wein, Tanita; Picazo, Devani Romero; Blow, Frances; Woehle, Christian; Jami, Elie; Reusch, Thorsten B.H.; Martin, William; Dagan, Tal

doi:10.1016/j.tim.2019.05.010

Cited by 35 publications

(25 citation statements)

References 131 publications

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“…The translocation or exchange of nutrients is a common feature of beneficial nutritional symbiosis [12]. The prevailing notion is that the sponge microbiome plays an important role in sponge health and nutrition [13] by extending the metabolic repertoire of the host [14,15].…”

Section: Introductionmentioning

confidence: 99%

Subcellular view of host–microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan–microbe symbiosis

et al. 2021

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Background Sponges are increasingly recognised as key ecosystem engineers in many aquatic habitats. They play an important role in nutrient cycling due to their unrivalled capacity for processing both dissolved and particulate organic matter (DOM and POM) and the exceptional metabolic repertoire of their diverse and abundant microbial communities. Functional studies determining the role of host and microbiome in organic nutrient uptake and exchange, however, are limited. Therefore, we coupled pulse-chase isotopic tracer techniques with nanoscale secondary ion mass spectrometry (NanoSIMS) to visualise the uptake and translocation of 13C- and 15N-labelled dissolved and particulate organic food at subcellular level in the high microbial abundance sponge Plakortis angulospiculatus and the low microbial abundance sponge Halisarca caerulea. Results The two sponge species showed significant enrichment of DOM- and POM-derived 13C and 15N into their tissue over time. Microbial symbionts were actively involved in the assimilation of DOM, but host filtering cells (choanocytes) appeared to be the primary site of DOM and POM uptake in both sponge species overall, via pinocytosis and phagocytosis, respectively. Translocation of carbon and nitrogen from choanocytes to microbial symbionts occurred over time, irrespective of microbial abundance, reflecting recycling of host waste products by the microbiome. Conclusions Here, we provide empirical evidence indicating that the prokaryotic communities of a high and a low microbial abundance sponge obtain nutritional benefits from their host-associated lifestyle. The metabolic interaction between the highly efficient filter-feeding host and its microbial symbionts likely provides a competitive advantage to the sponge holobiont in the oligotrophic environments in which they thrive, by retaining and recycling limiting nutrients. Sponges present a unique model to link nutritional symbiotic interactions to holobiont function, and, via cascading effects, ecosystem functioning, in one of the earliest metazoan–microbe symbioses.

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Section: Introductionmentioning

confidence: 99%

Subcellular view of host–microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan–microbe symbiosis

et al. 2021

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“…The currency exchanged (Wein et al, 2019) between the ancestral cockroach and its flagellates depends on knowing the physiological basis of the symbiotic partnership, a difficulty given the complex cocktail of metabolites involved and the derived nature of the microbiome in extant members of the lineage. Nonetheless, many animal groups produce cellulases on their own, but these are generally incomplete and must be supplemented by symbiotic microorganisms (Lo et al, 2003b.…”

Section: Parasitism To Mutualismmentioning

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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“…Protist-bacteria interactions range from mutualistic (e.g. metabolic exchange or scavenging of toxic compounds [19,20]), to antagonistic interplay that mainly comprises predation [18][19][20]. Top-down control via predation is thought to be the main cause of bacterial mortality in microbial ecosystems, and was shown to greatly impact community structure, composition and even affecting bacterial morphology and evolution [18].…”

Section: Introductionmentioning

confidence: 99%

Protozoa populations are ecosystem engineers that shape prokaryotic community structure and function of the rumen microbial ecosystem

Solomon

Wein

Levy

et al. 2020

Preprint

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Currency, Exchange, and Inheritance in the Evolution of Symbiosis

Cited by 35 publications

References 131 publications

Subcellular view of host–microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan–microbe symbiosis

Subcellular view of host–microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan–microbe symbiosis

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

Protozoa populations are ecosystem engineers that shape prokaryotic community structure and function of the rumen microbial ecosystem

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