Genomic Evidence for Phototrophic Oxidation of Small Alkanes in a Member of the Chloroflexi Phylum
Year: 2019
Type: article
Abstract: Recent genomic and microcosm based studies revealed a wide diversity of previously unknown microbial processes involved in alkane and methane metabolism. Here we described a new bacterial genome from a member of the Chloroflexi phylum—termed here Candidatus Chlorolinea photoalkanotrophicum—with cooccurring pathways for phototrophy and the oxidation of methane and/or other small alkanes. Recovered as a metagenome-assembled genome from microbial mats in an iron-rich hot spring in Japan, Ca. ‘C. photoalkanotrophicum’ forms a new lineage within the Chloroflexi phylum and expands the known metabolic diversity of this already diverse clade. Ca. ‘C. photoalkanotrophicum’ appears to be metabolically versatile, capable of phototrophy (via a Type 2 reaction center), aerobic respiration, nitrite reduction, oxidation of carbon monoxide, oxidation and incorporation of carbon from methane and/or other short-chain alkanes such as propane, and potentially carbon fixation via a novel pathway composed of hybridized components of the serine cycle and the 3-hydroxypropionate bi-cycle. The biochemical network of this organism is constructed from components from multiple organisms and pathways, further demonstrating the modular nature of metabolic machinery and the ecological and evolutionary importance of horizontal gene transfer in the establishment of novel pathways.
Language: English
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: green
Funders: National Science Foundation, National Aeronautics and Space Administration, California Institute of Technology, Agouron Institute, Eidgenössische Technische Hochschule Zürich, Japan Society for the Promotion of Science, National Institutes of Natural Sciences, Office of International Science and Engineering
Awards: OXYGENIC PHOTOSYNTHESIS IS PERHAPS THE MOST TRANSFORMATIVE BIOENERGETIC INNOVATION IN THE HISTORY OF LIFE AS THE ACTIVITY THAT FUNDAMENTALLY CHANGED THE PLANET. THE CARBON CYCLE WAS STIMULATED BY AN INCREASE IN PRIMARY PRODUCTIVITY RESULTING IN CASCADES OF EVOLUTIONARY INNOVATIONS. O2 BECAME WIDELY AVAILABLE FOR UTILIZATION AS AN OXIDANT IN ENERGY METABOLISM AND IN DIVERSE ANABOLIC AND CATABOLIC PATHWAYS. GEOCHEMICAL CYCLES WERE ALSO GREATLY ALTERED LEADING TO THE ACCUMULATION OF OTHER OXIDANTS IN THE ATMOSPHERE AND OCEANS. THE AVAILABILITY OF O2 ULTIMATELY LED TO AEROBIC RESPIRATION EUKARYOTIC ENDOSYMBIOSIS AND COMPLEX MULTICELLULARITY. NOT SURPRISINGLY THE PRESENCE OF ABUNDANT ATMOSPHERIC O2 FORMS PART OF OUR SEARCH IMAGE FOR LIFE ON PLANETS OUTSIDE OF OUR SOLAR SYSTEM.ALL EVIDENCE SUPPORTS THE THEORY THAT OXYGENIC PHOTOSYNTHESIS EVOLVED BUT ONCE IN AN ANOXYGENIC ANCESTOR OF MODERN CYANOBACTERIA. HOWEVER DETAILS OF THE EVOLUTIONARY STEPS TAKEN DURING THE RISE OF OXYGENIC PHOTOSYNTHESIS REMAIN A MYSTERY. A BETTER UNDERSTANDING OF THE NATURAL HISTORY OF THE PHYLUM MARKS A PATH FORWARD. ARE LINEAGES OF BACTERIA THAT SHARE THE SAME PRE-PHOTOTROPHIC ANCESTOR AS THE CYANOBACTERIA EXTANT TODAY? MIGHT BEHAVIOR OF THESE CELLS INFORM THE PHYSIOLOGICAL PLATFORM UPON WHICH OXYGENIC PHOTOTROPHY EVOLVED?ENVIRONMENTAL SEQUENCING EFFORTS ILLUSTRATE THAT CYANOBACTERIA ARE MORE DIVERSE THAN HISTORICALLY APPRECIATED. SEVERAL UNCHARACTERIZED CLADES OF DEEP BRANCHING FORMS EXIST; MOREOVER THESE OCCUR IN PERENNIALLY DARK AND OFTEN ANOXIC ENVIRONMENTS WHICH SUGGESTS THAT THE CORRESPONDING ORGANISMS ARE NOT OXYPHOTOTROPHS (1). RECENT GENOME ANALYSES ON UNCULTIVATED REPRESENTATIVES OF ONE OF THESE 'DARK CYANOBACTERIA' CLADES (TERMED MELAINABACTERIA) REVEALED NO GENES ASSOCIATED WITH PHOTOSYNTHESIS (2 3); NEARLY ALL LACKED GENES FOR AEROBIC OR ANAEROBIC RESPIRATION. THUS MELAINABACTERIA AND OTHER NEWLY IDENTIFIED CLADES OF 'DARK CYANOBACTERIA' PROVIDE IMPORTANT INSIGHTS INTO THE ORGANISMS FROM WHICH OXYGENIC PHOTOSYNTHESIS AROSE.PILOT RESEARCH AT CALTECH IDENTIFIED AN ENVIRONMENT WHEREIN SEVERAL DIFFERENT LINEAGES OF DARK CYANOBACTERIA ARE RELIABLY AND REPRODUCIBLY RESIDING: THE COMPLEX FERMENTATION-DRIVEN GUT MICROBIAL COMMUNITIES OF TERMITES. THIS MODEL ENVIRONMENT IS PARTICULARLY ATTRACTIVE FOR LABORATORY-BASED STUDIES BECAUSE IT IS A MICROLITER IN VOLUME WELL-BOUNDED AVAILABLE IN LARGE NUMBERS OF REPLICATES AND STRAIGHTFORWARD TO MAINTAIN IN THE LABORATORY. PILOT EXPERIMENTS REVEAL THAT A SINGLE TERMITE HINDGUT CONTAINS AT LEAST FOUR INDEPENDENT CLADES OF THE DARK CYANOBACTERIA - THE HIGHEST AND DEEPEST DIVERSITY OBSERVED IN ANY ENVIRONMENT TO DATE. WE PROPOSE A DETAILED AND MULTIDISCIPLINARY STUDY OF THESE DARK CYANOBACTERIA USING ENVIRONMENTAL PERTURBATIONS COMPARATIVE METAGENOMICS AND TRANSCRIPTOMICS FISH AND OTHER MICROSCALE LOCALIZATION APPROACHES AS WELL AS PHYSIOLOGICAL LINES. COMPARATIVE GENEBASED ANALYSES OF DARK CYANOBACTERIAL DIVERSITY IN DIFFERENT TERMITE SPECIES REPRESENTING DISTINCT INSECT FAMILY LINEAGES WILL ALSO BE PERFORMED OFFERING A VIEW INTO EVOLUTIONARY RATES AND PATTERNS OF DIVERSIFICATION IN DARK CYANOBACTERIA [I.E. IN THE CONTEXT OF THE 100+ MILLION YEAR FOSSIL RECORD OF TERMITES AND OTHER METADATA ON THE HOSTS (4)].THE PROPOSED SCOPE FITS SEVERAL PROGRAM OBJECTIVES. FOR EXAMPLE EARLY EVOLUTION OF LIFE AND THE BIOSPHERE AIMS TO 'UNDERSTAND THE PHYLOGENY AND PHYSIOLOGY OF MICROORGANISM - WHOSE CHARACTERISTICS MAY REFLECT THE NATURE OF PRIMITIVE ENVIRONMENTS ' 'INVESTIGATE THE DEVELOPMENT OF KEY BIOLOGICAL PROCESSES AND THEIR ENVIRONMENTAL IMPACT ' AND 'INVESTIGATE THE EVOLUTION OF GENES PATHWAYS AND MICROBIAL SPECIES SUBJECT TO LONG-TERM ENVIRONMENTAL CHANGE.'1. F. WARNECKE ET AL. NATURE 450 560-565 (2007).2. S. C. DI RIENZI ET AL. ELIFE 2:E01102 (2013).3. R. M. SOO ET AL. GENOME BIOL EVOL 6 1031 (2014).4. X. ZHANG J.R. LEADBETTER (2012) MBIO 3:E00223-12 (2012)., Determining sulfur isotope fractionation values of individual enzymes and how they evolve through time., AEROBIC RESPIRATION THE ABILITY TO COUPLE THE REDUCTION OF MOLECULAR OXYGEN TO THE OXIDATION OF REDUCED COMPOUNDS WHILE CONSERVING ENERGY TO DRIVE CELLULAR PROCESSES IS THE MOST WIDESPREAD AND BIOENERGETICALLY FAVORABLE METABOLISM ON EARTH TODAY. AEROBIC RESPIRATION IS ESSENTIAL FOR THE DEVELOPMENT OF COMPLEX LIFE AND SO THE PRESENCE OF ABUNDANT MOLECULAR OXYGEN IS A CRUCIAL COMPONENT OF PLANETARY HABITABILITY. O2 ON EARTH IS SUPPLIED BY OXYGENIC PHOTOSYNTHESIS BUT IT IS BECOMING MORE WIDELY UNDERSTOOD THAT OTHER ABIOTIC PROCESSES MAY SUPPLY SMALL AMOUNTS OF O2 ON OTHER WORLDS BUT IT IS NOT YET CLEAR WHETHER THESE SOURCES ARE SUFFICIENT FOR AEROBIC ORGANISMS. IN THE MARTIAN ATMOSPHERE O2 IS IN VERY LOW ABUNDANCE BUT A GROWING NUMBER OF OBSERVATIONS SUGGEST THAT IT MAY HAVE BEEN HIGHER IN THE PAST PERHAPS WHEN MARS POSSESSED A THICKER ATMOSPHERE. THE RECENTLY REPORTED DISCOVERY OF MANGANESE OXIDES IN ANCIENT MARTIAN SEDIMENTARY ROCKS POINTS TO HIGHER O2 LEVELS IN AQUEOUS ENVIRONMENTS SOMETIME IN MARS HISTORY. MY EXPERIMENTS WITH SPONGES HAVE DEMONSTRATED THAT LOW-MICROMOLAR OXYGEN CONCENTRATIONS ARE SUFFICIENT TO SUPPORT SIMPLE ANIMALS WHILE SIMILAR EXPERIMENTS WITH THE BACTERIUM ESCHERICHIA COLI DEMONSTRATED GROWTH AT O2 LEVELS THREE ORDERS OF MAGNITUDE LOWER. THIS RAISES THE IMPORTANT QUESTION OF WHETHER OR NOT ANCIENT MARS HAD SUFFICIENT AMOUNTS OF OXYGEN TO AT LEAST IN PRINCIPLE SUPPORT AEROBIC ORGANISMS. TO ADDRESS THIS AN IMPROVED UNDERSTANDING OF THE LIMITING CONCENTRATIONS OF O2 REQUIRED FOR RESPIRATION AS WELL AS THE DISTRIBUTION AND HISTORY OF OXYGEN ON MARS IS NECESSARY TO TEST THE POSSIBILITY OF AEROBIOSIS ON OTHER WORLDS. I PROPOSE AN EXPERIMENTAL APPROACH TO DEVELOP A QUANTITATIVE FRAMEWORK FOR EVALUATING THE HABITABILITY OF PLANETARY BODIES FOR AEROBIC ORGANISMS USING MARS AS A CASE STUDY. TO ACCOMPLISH THIS I HAVE DESIGNED TWO DISCRETE BUT COMPLEMENTARY ACTIVITIES: 1) LABORATORY EXPERIMENTS TO QUANTIFY THE LIMITS OF AEROBIC RESPIRATION IN MICROBIAL MODEL ORGANISMS (USING DISTINCT O2-REDUCING PATHWAYS) AND 2) MEASUREMENTS OF MANGANESE OXIDATION AT LOW OXYGEN CONCENTRATIONS TO AID IN THE INTERPRETATION OF PAST O2 CONCENTRATIONS FROM OBSERVATIONS OF THE MARTIAN GEOLOGICAL RECORD AND EVALUATE WHETHER THESE ANCIENT ENVIRONMENTS WOULD HAVE BEEN HABITABLE FOR AEROBES. THIS STUDY WILL EMPLOY A NOVEL EXPERIMENTAL TECHNIQUE THAT COUPLES HIGHLY SENSITIVE MICROELECTRODES WITH A MICRORESPIRATION APPARATUS TO MEASURE O2 CONCENTRATIONS PRECISELY AND IN REAL-TIME. RESULTS FROM THESE EXPERIMENTS COMBINED WITH OBSERVATIONS OF MANGANESE IN THE STRATA EXPOSED AT THE BASE OF MT. SHARP IN GALE CRATER ON MARS VIA THE CURIOSITY ROVER WILL ASSESS THE OPPORTUNITIES FOR AEROBIC LIFE IN MARS PAST. THIS WORK WILL BROADEN OUR UNDERSTANDING OF OXYGEN AND THE METABOLIC OPPORTUNITIES FOR AEROBES ON OTHER PLANETARY BODIES PARTICULARLY THOSE WHERE O2 FLUXES ARE NOT SOURCED FROM AND CONTINGENT UPON PHOTOSYNTHETIC ORGANISMS AS THEY ARE ON EARTH., Graduate Research Fellowship Program (GRFP), Collaborative Research: Biochemical, Genetic, Metabolic and Isotopic Constraints on an Ancient Thiobiosphere, Dissertation Enhancement: Investigating Chloroflexi mats at a Japanese Hot Spring as a Model for Anoxygenic Stromatolites
OpenAlex ID: W3102109885