Carbon assimilation strategies in ultrabasic groundwater: clues from the integrated study of a serpentinization-influenced aquifer

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Seyler, L. M., Brazelton, W. J., McLean, C., Putman, L. I., Hyer, A., Kubo, M. D. Y., Hoehler, T., Cardace, D., & Schrenk, M. O. . Carbon assimilation strategies in ultrabasic groundwater: clues from the integrated study of a serpentinization-influenced aquifer. mSystems, 5(2), (2020): e00607-00619, doi: 10.1128/mSystems.00607-19.Serpentinization is a low-temperature metamorphic process by which ultramafic rock chemically reacts with water. Such reactions provide energy and materials that may be harnessed by chemosynthetic microbial communities at hydrothermal springs and in the subsurface. However, the biogeochemistry mediated by microbial populations that inhabit these environments is understudied and complicated by overlapping biotic and abiotic processes. We applied metagenomics, metatranscriptomics, and untargeted metabolomics techniques to environmental samples taken from the Coast Range Ophiolite Microbial Observatory (CROMO), a subsurface observatory consisting of 12 wells drilled into the ultramafic and serpentinite mélange of the Coast Range Ophiolite in California. Using a combination of DNA and RNA sequence data and mass spectrometry data, we found evidence for several carbon fixation and assimilation strategies, including the Calvin-Benson-Bassham cycle, the reverse tricarboxylic acid cycle, the reductive acetyl coenzyme A (acetyl-CoA) pathway, and methylotrophy, in the microbial communities inhabiting the serpentinite-hosted aquifer. Our data also suggest that the microbial inhabitants of CROMO use products of the serpentinization process, including methane and formate, as carbon sources in a hyperalkaline environment where dissolved inorganic carbon is unavailable.We thank McLaughlin Reserve, in particular Paul Aigner and Cathy Koehler, for hosting sampling at CROMO and providing access to the wells, A. Daniel Jones and Anthony Schilmiller for their advice regarding metabolite extraction and mass spectrometry, Elizabeth Kujawinski for her guidance in metabolomics data analysis and interpretation, and Julia McGonigle, Christopher Thornton, and Katrina Twing for assistance with metagenomic and computational analyses

The compositional and evolutionary logic of metabolism

Metabolism displays striking and robust regularities in the forms of modularity and hierarchy, whose composition may be compactly described. This renders metabolic architecture comprehensible as a system, and suggests the order in which layers of that system emerged. Metabolism also serves as the foundation in other hierarchies, at least up to cellular integration including bioenergetics and molecular replication, and trophic ecology. The recapitulation of patterns first seen in metabolism, in these higher levels, suggests metabolism as a source of causation or constraint on many forms of organization in the biosphere. We identify as modules widely reused subsets of chemicals, reactions, or functions, each with a conserved internal structure. At the small molecule substrate level, module boundaries are generally associated with the most complex reaction mechanisms and the most conserved enzymes. Cofactors form a structurally and functionally distinctive control layer over the small-molecule substrate. Complex cofactors are often used at module boundaries of the substrate level, while simpler ones participate in widely used reactions. Cofactor functions thus act as "keys" that incorporate classes of organic reactions within biochemistry. The same modules that organize the compositional diversity of metabolism are argued to have governed long-term evolution. Early evolution of core metabolism, especially carbon-fixation, appears to have required few innovations among a small number of conserved modules, to produce adaptations to simple biogeochemical changes of environment. We demonstrate these features of metabolism at several levels of hierarchy, beginning with the small-molecule substrate and network architecture, continuing with cofactors and key conserved reactions, and culminating in the aggregation of multiple diverse physical and biochemical processes in cells.Comment: 56 pages, 28 figure

Prospective organisation of neonatal arm movements : a motor foundation of embodied agency, disrupted in premature birth

Prospective motor control moves the body into the future, from where one is to where one wants to be. It is a hallmark of intentionality. But its origins in development is uncertain. In this study, we tested whether or not the arm movements of newborn infants were prospectively controlled. We measured the spatiotemporal organisation of 480 neonatal arm movements and 384 arm movements of infants prematurely born at-risk for neurodevelopmental disorder. We found 75% of healthy term-birth neonatal movements and 68% of prematurely-born infant movements conformed to the tauG-coupling model of prospective sensorimotor control. Prospective coupling values were significantly reduced in the latter (p = .010, r = .087). In both cases prospectively controlled movements were tightly organised by fixed-duration units with a base duration of 218 ms and additional temporal units of 145 ms. Yet distances remained constant. Thus, we demonstrate for the first time a precise prospective spatiotemporal organisation of neonatal arm movements and demonstrate at-risk infants exhibit reduced sensorimotor control. Prospective motor control is a hallmark of primary sensorimotor intentionality and gives a strong embodied foundation to conscious motor agency

Mother-to-infant and father-to-infant initial emotional involvement

While infant attachment has been largely studied, parental attachment is still relatively unknown, especially when referred to fathers. However, it is mainly recognised that parents’ emotional involvement with the newborn contributes to the quality of the interaction and the care they provide. The aim of this study was to study mother-to-infant and father-to-infant initial emotional involvement; namely, differences between mothers and fathers and changes in mother’s emotions toward the neonate within the first days after delivery. The Bonding Scale, an extended Portuguese version of the ‘New Mother-to-Infant Bonding Scale’, was administered during the first two days after childbirth to a sample of 315 mothers and 141 fathers (n = 456), at the Júlio Dinis Maternity Hospital (Portugal). Most mothers and fathers show positive emotions and only a few of them showed negative emotions toward the infant. Maternal and paternal emotional involvement toward the newborn tend to be similar; nevertheless, fathers show less fear and better emotional involvement with the neonate, while mothers are sadder and show more emotions not related to bonding. During the first days following delivery, emotions not related to bonding, such as fear, seem to decrease in mothers.Bial Foundation - Grant 58/02.Human Development and Health Service of the Calouste Gulbenkian Foundation - Grant 48914

Infants’ behavioral and physiological profile and mother–infant interaction

This study aims to (a) identify and profile groups of infants according to their behavioral and physiological characteristics, considering their neurobehavioral organization, social withdrawal behavior, and endocrine reactivity to stress, and to (b) analyze group differences in the quality of mother–infant interaction. Ninety seven 8-week-old infants were examined using the Neonatal Behavioral Assessment Scale and the Alarm Distress Baby Scale. Cortisol levels were measured both before and after routine inoculation between 8 and 12 weeks. At 12 to 16 weeks mother–infant interaction was assessed using the Global Rating Scales of Mother–Infant Interaction. Three groups of infants were identified: (a) ‘‘withdrawn’’; (b) ‘‘extroverted’’; (c) ‘‘underaroused.’’ Differences between them were found regarding both infant and mother behaviors in the interaction and the overall quality of mother–infant interaction. The identification of behavioral and physiological profiles in infants is an important step in the study of developmental pathways

Parent–Infant Room Sharing During the First Months of Life: Longitudinal Links With Behavior During Middle Childhood

Current recommendations encourage parent–infant room sharing for the first 6 months of life. This longitudinal study (N = 193) is the first to examine long-term relations of early room sharing with three domains of child behavior: sleep, behavior problems, and prosocial behavior. Information on room sharing was collected daily for infants’ first 6 months. At ages 6, 7, and 8 years, outcomes were assessed with maternal and teacher questionnaires and behavioral observations. Early room sharing was not related to sleep problems or behavior problems. Additionally, more weeks of room sharing were positively related to higher maternal ratings of child sleep quality and more prosocial behavior. In conclusion, early room sharing appears to be related to positive, but not negative, behavior outcomes in middle childhood.https://doi.org/10.1111/cdev.1314

Measuring the quality and quantity of professional intrapartum support: Testing a computerised systematic observation tool in the clinical setting

Background: Continuous support in labour has a significant impact on a range of clinical outcomes, though whether the quality and quantity of support behaviours affects the strength of this impact has not yet been established. To identify the quality and quantity of support, a reliable means of measurement is needed. To this end, a new computerised systematic observation tool, the ‘SMILI' (Supportive Midwifery in Labour Instrument) was developed. The aim of the study was to test the validity and usability of the ‘Supportive Midwifery in Labour Instrument' (SMILI) and to test the feasibility and acceptability of the systematic observation approach in the clinical intrapartum setting. Methods: Systematic observation was combined with a postnatal questionnaire and the collection of data about clinical processes and outcomes for each observed labour. The setting for the study was four National Health Service maternity units in Scotland, UK. Participants in this study were forty five midwives and forty four women. The SMILI was used by trained midwife observers to record labour care provided by midwives. Observations were undertaken for an average of two hours and seventeen minutes during the active first stage of labour and, in 18 cases, the observation included the second stage of labour. Content validity of the instrument was tested by the observers, noting the extent to which the SMILI facilitated the recording of all key aspects of labour care and interactions. Construct validity was tested through exploration of correlations between the data recorded and women's feelings about the support they received. Feasibility and usability data were recorded following each observation by the observer. Internal reliability and construct validity were tested through statistical analysis of the data. Results: One hundred and four hours of labour care were observed and recorded using the SMILI during forty nine labour episodes. Conclusion: The SMILI was found to be a valid and reliable instrument in the intrapartum setting in which it was tested. The study identified that the SMILI could be used to test correlations between the quantity and quality of support and outcomes. The systematic observational approach was found to be an acceptable and feasible method of enquiry

Metagenomic Identification of Active Methanogens and Methanotrophs in Serpentinite Springs of the Voltri Massif, Italy

The production of hydrogen and methane by geochemical reactions associated with the serpentinization of ultramafic rocks can potentially support subsurface microbial ecosystems independent of the photosynthetic biosphere. Methanogenic and methanotrophic microorganisms are abundant in marine hydrothermal systems heavily influenced by serpentinization, but evidence for methane-cycling archaea and bacteria in continental serpentinite springs has been limited. This report provides metagenomic and experimental evidence for active methanogenesis and methanotrophy by microbial communities in serpentinite springs of the Voltri Massif, Italy. Methanogens belonging to family Methanobacteriaceae and methanotrophic bacteria belonging to family Methylococcaceae were heavily enriched in three ultrabasic springs (pH 12). Metagenomic data also suggest the potential for hydrogen oxidation, hydrogen production, carbon fixation, fermentation, and organic acid metabolism in the ultrabasic springs. The predicted metabolic capabilities are consistent with an active subsurface ecosystem supported by energy and carbon liberated by geochemical reactions within the serpentinite rocks of the Voltri Massif