Biology subjects

Seminara, A.

Publications and source records attributed to Seminara, A..

6 recordsLinked to original sources

bioRxiv2023

Evolution of novel sensory organs in fish with legs

How do animals evolve new traits? Sea robins are unusual "walking" fishes that use leg-like appendages to navigate the seafloor. Here, we show that legs are bona fide sense organs that mediate the unique ability to localize and uncover buried prey. We then probe the developmental and physiological basis of these novel sense organs as a striking example of a major trait gain in evolution. We find certain sea robin species have legs with unique end-organs called papillae that mediate enhanced mechanical and chemical sensitivity to enable predatory digging behavior. Papillae exhibit dense innervation from touch-sensitive neurons, noncanonical epithelial taste receptors, and chemical sensitivity that drives predatory digging behavior. Using a combination of developmental analyses, crosses between species with and without papillae, and interspecies comparisons of sea robins from around the world, we demonstrate that papillae represent a key evolutionary innovation associated with behavioral niche expansion on the seafloor. These discoveries provide a conceptual framework for understanding how molecular, cellular, and tissue-scale adaptations integrate to produce novel organismic traits and behavior.

evolutionary biology↗

bioRxiv2023

Reconstitution of ORP-mediated lipid exchange process coupled to PI(4)P metabolism

Lipid distribution in the eukaryotic cells depends on tight couplings between lipid transfer and lipid metabolism. Yet these couplings remain poorly described. Notably, it is unclear to what extent lipid exchangers of the OSBP-related proteins (ORPs) family, coupled to PI(4)P metabolism, contribute to the formation of sterol and phosphatidylserine gradient between the endoplasmic reticulum (ER) and other cell regions. To address this question, we have examined in vitro the activity of Osh4p, a representative ORP, between Golgi mimetic membranes in which PI(4)P is produced by a PI 4-kinase and ER mimetic membranes in which PI(4)P is hydrolyzed by the phosphatase Sac1p. Using quantitative, real-time assays, we demonstrate that Osh4p creates a sterol gradient between the two membranes by sterol/PI(4)P exchange as soon as a PI(4)P gradient is generated at this interface following ATP addition, and define how much PI(4)P must be synthesized for this process. Then, using a kinetic model supported by our in vitro data, we estimate to what extent PI(4)P metabolism can drive lipid transfer in cells. Finally, we show that Sec14p, by transferring phosphatidylinositol between membranes, can support the synthesis of PI(4)P and the creation of a sterol gradient by Osh4p. These results indicate to what extent ORPs, under the control of PI(4)P metabolism, can distribute lipids in the cell.

biochemistry↗

bioRxiv2023

Molecular tuning of sea anemone stinging

Jellyfish and sea anemones fire single-use, venom-covered barbs to immobilize prey or predators. We previously showed that the anemone Nematostella vectensis uses a specialized voltage-gated calcium (CaV) channel to trigger stinging in response to synergistic prey-derived chemicals and touch (Weir et al., 2020). Here we use experiments and theory to find that stinging behavior is suited to distinct ecological niches. We find that the burrowing anemone Nematostella uses uniquely strong CaV inactivation for precise control of predatory stinging. In contrast, the related anemone Exaiptasia diaphana inhabits exposed environments to support photosynthetic endosymbionts. Consistent with its niche, Exaiptasia indiscriminately stings for defense and expresses a CaV splice variant that confers weak inactivation. Chimeric analyses reveal that CaV{beta} subunit adaptations regulate inactivation, suggesting an evolutionary tuning mechanism for stinging behavior. These findings demonstrate how functional specialization of ion channel structure contributes to distinct organismal behavior.

physiology↗

bioRxiv2023

Differences in spore size and atmospheric survival shape stark contrasts in the dispersal dynamics of two closely related fungal pathogens

A frequently ignored but critical aspect of microbial dispersal is survival in the atmosphere. We exposed spores of two closely related, morphologically dissimilar, and economically important fungal pathogens to typical atmospheric environments and modeled their movement in the troposphere. We first measured the mortality of Alternaria solani and A. alternata conidia exposed to ranges of solar radiation, relative humidity, and temperature. We then measured survival in an advantageous environment over 12 days. A. solani conidia are nearly 10 times larger than A. alternata conidia and most die after 24 hours. By contrast, over half of A. alternata conidia remained viable at 12 days. The greater viability of the smaller spores is counterintuitive as larger spores are assumed to be more durable. To elucidate the consequences of survival rates for dispersal, we deployed models of atmospheric spore movement across North American. We predict 99% of the larger A. solani conidia settle within 24 hours, with a maximum dispersal distance of 100 km. By contrast, most A. alternata conidia remain airborne for more than 12 days and long-distance dispersal is possible, e.g., from Wisconsin to the Atlantic Ocean. We observe that the larger conidia of A. solani survive poorly but also land sooner and move over shorter distances as compared to the smaller conidia of A. alternata. Our data relating larger spore size to poorer survival in the atmosphere and shorter distances travelled likely translate to other fungal species and highlight the potential for starkly different dispersal dynamics among even closely related fungi.

microbiology↗

bioRxiv2021

Alternation emerges as a multi-modal strategy for turbulent odor navigation

Foraging mammals exhibit a familiar yet poorly characterized phenomenon, "alternation", a momentary pause to sniff in the air often preceded by the animal rearing on its hind legs or raising its head. Intriguingly, rodents executing an olfactory search task spontaneously exhibit alternation in the presence of airflow, suggesting that alternation may serve an important role during turbulent plume-tracking. To test this hypothesis, we combine fully-resolved numerical simulations of turbulent odor transport and Bellman optimization methods for decision-making under partial observability. We show that an agent trained to minimize search time in a realistic odor plume exhibits extensive alternation together with the characteristic cast-and-surge behavior commonly observed in flying insects. Alternation is tightly linked with casting and occurs more frequently when the agent is far downwind of the source, where the likelihood of detecting airborne cues is higher relative to cues close to the ground. Casting and alternation emerge as complementary tools for effective exploration when cues are sparse. We develop a model based on marginal value theory to capture the interplay between casting, surging and alternation. More generally, we show how multiple sensorimotor modalities can be fruitfully integrated during complex goal-directed behavior.

animal behavior and cognition↗

bioRxiv2020

Plume dynamics structure the spatiotemporal activity of glomerular networks in the mouse olfactory bulb

Although mice locate resources using turbulent airborne odor plumes, the stochasticity and intermittency of fluctuating plumes create challenges for interpreting odor cues in natural environments. Population activity within the olfactory bulb (OB), is thought to process this complex spatial and temporal information, but how plume dynamics impact odor representation in this early stage of the mouse olfactory system is not known. Limitations in odor detection technology have made it impossible to measure plume fluctuations while simultaneously recording from the mouses brain. Thus, previous studies have measured OB activity following controlled odor pulses of varying profiles or frequencies, but this approach only captures a subset of features found within olfactory plumes. Adequately sampling this feature space is difficult given a lack of knowledge regarding which features the brain extracts during exposure to natural olfactory scenes. Here we measured OB responses to naturally fluctuating odor plumes using a miniature, adapted odor sensor combined with wide-field GCaMP6f signaling from the dendrites of mitral and tufted (MT) cells imaged in olfactory glomeruli of head-fixed mice. We precisely tracked plume dynamics and imaged glomerular responses to this fluctuating input, while varying flow conditions across a range of ethologically-relevant values. We found that a consistent portion of MT activity in glomeruli follows odor concentration dynamics, and the strongest responding glomeruli are the best at following fluctuations within odor plumes. Further, the reliability and average response magnitude of glomerular populations of MT cells are affected by the flow condition in which the animal samples the plume, with the fidelity of plume following by MT cells increasing in conditions of higher flow velocity where odor dynamics result in intermittent whiffs of stronger concentration. Thus, the flow environment in which an animal encounters an odor has a large-scale impact on the temporal representation of an odor plume in the OB. Additionally, across flow conditions odor dynamics are a major driver of activity in many glomerular networks. Taken together, these data demonstrate that plume dynamics structure olfactory representations in the first stage of odor processing in the mouse olfactory system.

neuroscience↗