Search bioRxiv⌕ Search

Biology subjects

Carrier, T. J.

Publications and source records attributed to Carrier, T. J..

6 recordsLinked to original sources

Temperature-induced shift in the rare microbiota of the sponge Haliclona

Ocean warming is currently leading to distributional shifts of species and an alternation of coastal communities. Vulnerable species that are most sensitive to ocean warming are able to use several acclimation mechanisms, with one of the fastest being a shift in and shuffling of their partnerships with symbiotic microorganisms. Assessing symbiosis-focused mechanisms of acclimation and adaptation in response to ocean warming is a technical challenge due to the difficulty of accurately simulating the de novo formation of coastal communities. Here, we use the Kiel Outdoor Benthocosm facility to assess which sponges species are experimentally recruited and whether they exhibit symbiosis-focused mechanisms of acclimation following selection to ocean warming. We observed one sponge species (Haliclona sp.) and found that this sponge exhibited significant shifts in the membership and composition of its associated microbiome in response to ocean warming, with much of this being attributed to the rare microbiota. Moreover, Haliclona sp. maintained the diversity and dominance of its microbiome members. Four bacteria taxa were differentially abundant at elevated temperatures, with two being a Francisella sp. that is a suspected pathogen and an uncultured Francisellaceae that is most closely related to sulfur-oxidizing endosymbionts. Changes to the Haliclona sp. microbiome are largely consistent with a limited acclimation response, which could indicate that this sponge may use microbial symbionts as part of a mechanism to acclimate and adapt to a warmer future ocean.

ecology↗

Maternal transmission of a plastid structure enhances offspring fitness

Development in the sea has long been thought to be a nutritional gamble that disproportionately ends in starvation. Here, we unexpectedly show that components of plastids are incorporated into sea urchin eggs and that these, in turn, benefit developmental fitness. We find chromoplast-derived carotenoid crystals and chromoplast-specific metabolites inside of sea urchin eggs. The light-dependent activity of these chromoplast components influence the subsequent abundance of phytohormones that, in turn, regulate the use of energetic lipids that promote development and survival. Offspring that benefit from these chromoplast components are predicted to disperse further, over larger geographic areas, and use a wider range of currents, including those that cross ocean basins. Data presented here challenge the long-held assumption that components of non-metazoan organelles are unable to enter the germline and be passed between generations. We hypothesize that sea urchins manipulate plastids solely for their self-interest by a process that we term machioplasty, with the result of this process being a novel and adaptive form of maternal provisioning. SIGNIFICANCEMaking a fertilizable egg is a complex and carefully regulated process. One long-held assumption is that any component of non-animal organelles are unable to cross the evolutionary valley between non-reproductive and reproductive cells. Here, we unexpectedly show that components of plastids are incorporated into sea urchin eggs and that these, in turn, benefit developmental fitness. Offspring benefit from these plastid components by developing more quickly into larvae and having higher survival due to ability to use phytohormones that influence energetic lipids. This allows offspring to use a wider range of ocean currents, including those that cross entire basins. This challenge the long-held assumption that components of non-metazoan organelles are unable to be passed between generations.

developmental biology↗

Microbes as manipulators of developmental life-history

Marine invertebrates mainly reproduce by energy-poor eggs that develop into feeding larvae or energy-rich eggs that develop into non-feeding larvae1-4. Transitions between these reproductive strategies have been studied in detail5-7, yet the evolutionary factor(s) responsible for these switches remains elusive. Here, we use theoretical models to show that microbes with the capacity to manipulate host reproduction are one possible factor. We report that microbial manipulators create a sperm-limited environment that selects for larger eggs by shifting the hosts sex ratio towards female dominance and, as a result, serve as the evolutionary driver of transitions in the developmental life-history for marine invertebrates. Loss of a microbial manipulator can then recover the ancestral developmental life-history. We also document more than a dozen genera of marine invertebrates from throughout the worlds oceans that fit the framework of a microbe-induced switch between these predominate reproductive strategies. We anticipate that microbial manipulators have a yet-to-be appreciated influence on the life-history strategies of marine invertebrates. We find it paramount to understand if transitions in developmental life-history also occur without microbial manipulators as well as if the underlying mechanisms of these manipulations are convergent with terrestrial systems.

evolutionary biology↗

Maternal provisioning of an obligate symbiont

Vertical transmission of microbial symbionts is interpreted as all offspring within a clutch being provided a similar number of symbionts irrespective of reproductive output (fecundity). This interpretation, however, stems primarily from oviparous insects and, thus, has yet to consider other major reproductive strategies. We used the viviparous sponge Halichondria panicea and its obligate symbiont "Candidatus Halichondribacter symbioticus" to test the hypothesis that offspring receive quantitatively similar numbers of its obligate symbiont. This quantitative strategy of vertical transmission was not observed. Instead, we find that H. panicea has a maternal pool of Ca. H. symbioticus that is partitioned proportionally to reproductive output and allometrically by offspring size. Moreover, Ca. H. symbioticus could not be experimentally reduced in larvae by antibiotics, while the total bacterial community could be depleted. The ability to undergo metamorphosis was unaffected by this perturbation. Together, this demonstrates that the obligate symbiont Ca. H. symbioticus is maternally provisioned and, thus, provides an additional strategy for how microbes can be vertically transmitted.

evolutionary biology↗

Divergent microbiota of echinoid eggs separated by the Isthmus of Panama

Relationships between animals and their associated microbiota is dependent on the evolutionary history of the host and on the environment. The majority of studies tend to focus on one of these factors and rarely consider how both determine the community composition of the associated bacteria. One "natural experiment" to test how evolutionary history, shared environments, and the interaction between these factors drive community composition is to compare geminate species pairs. Echinoids separated by the Isthmus of Panama are suitable for this comparison due to the known evolutionary history and differences in oceanographic characteristics of the Caribbean Sea and Pacific Ocean. By comparing the egg-associated microbiota for the Echinometra and Diadema geminate species pairs, we show that both pairs of geminate species associate with distinct bacterial communities in patterns consistent with phylosymbiosis, and that the interaction between the evolutionary history of the host and the environment best explain differences in these communities. Moreover, we find that particular microbial taxa differed considerably between, but not within, oceans and that the microbiota of the two Caribbean Echinometra species were dominated by the phototrophic Oxyphotobacteria.

ecology↗

A microbial perspective on the life-history evolution of marine invertebrate larvae: if, where, and when to feed

The feeding environment for planktotrophic larvae has a major impact on development and progression towards competency for metamorphosis. High phytoplankton environments that promote growth often have a greater microbial load and incidence of pathogenic microbes, while areas with lower food availability have a lower number of potential pathogens. Trade-offs between metabolic processes associated with growth and immune functionality have been described throughout the animal kingdom and may influence the life-history evolution of marine invertebrate planktotrophic larvae in these environments. Namely, to avoid potential incidences of microbial-mediated mortality and/or dysbiosis, larvae should regulate time spent between these two feeding environments. We describe here transcriptomic and microbiome data that supports this trade-off in larvae, where larvae in a well-fed environment upregulate genes associated with metabolism and may regularly enter a state of dysbiosis, resulting in mortality. To address the hypothesis that the environmental microbiota is a selective force on if, where, and when planktotrophic larvae should feed, we present a strategy for determining the specific interactions of larvae and microbes at a scale representative of their larger pelagic environment.

evolutionary biology↗