Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments

ABSTRACTEnergy-starved microbes in deep marine sediments subsist at near-zero growth for thousands of years, yet the mechanisms for their subsistence are unknown because no model strains have been cultivated from most of these groups. We investigated Baltic Sea sediments with single-cell genomics, metabolomics, metatranscriptomics, and enzyme assays to identify possible subsistence mechanisms employed by unculturedAtribacteria,Aminicenantes,Actinobacteriagroup OPB41,Aerophobetes,Chloroflexi,Deltaproteobacteria,Desulfatiglans,Bathyarchaeota, andEuryarchaeotamarine group II lineages. Some functions appeared to be shared by multiple lineages, such as trehalose production and NAD+-consuming deacetylation, both of which have been shown to increase cellular life spans in other organisms by stabilizing proteins and nucleic acids, respectively. Other possible subsistence mechanisms differed between lineages, possibly providing them different physiological niches. Enzyme assays and transcripts suggested thatAtribacteriaandActinobacteriagroup OPB41 catabolized sugars, whereasAminicenantesandAtribacteriacatabolized peptides. Metabolite and transcript data suggested thatAtribacteriautilized allantoin, possibly as an energetic substrate or chemical protectant, and also possessed energy-efficient sodium pumps.Atribacteriasingle-cell amplified genomes (SAGs) recruited transcripts for full pathways for the production of all 20 canonical amino acids, and the gene for amino acid exporter YddG was one of their most highly transcribed genes, suggesting that they may benefit from metabolic interdependence with other cells. Subsistence of uncultured phyla in deep subsurface sediments may occur through shared strategies of using chemical protectants for biomolecular stabilization, but also by differentiating into physiological niches and metabolic interdependencies.IMPORTANCEMuch of life on Earth exists in a very slow-growing state, with microbes from deeply buried marine sediments representing an extreme example. These environments are like natural laboratories that have run multi-thousand-year experiments that are impossible to perform in a laboratory. We borrowed some techniques that are commonly used in laboratory experiments and applied them to these natural samples to make hypotheses about how these microbes subsist for so long at low activity. We found that some methods for stabilizing proteins and nucleic acids might be used by many members of the community. We also found evidence for niche differentiation strategies, and possibly cross-feeding, suggesting that even though they are barely growing, complex ecological interactions continue to occur over ultralong timescales.

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Who is the “Matchmaker” between Proteins and Nucleic Acids?

10.20944/preprints202003.0419.v10 ◽

2021 ◽

Author(s):

Ping Xie

Keyword(s):

Nucleic Acids ◽

Genetic Code ◽

Photochemical Reactions ◽

Host Cells ◽

Darwinian Evolution ◽

Lipid Vesicle ◽

Biochemical System ◽

Cellular Life ◽

Biochemical Systems ◽

Life On Earth

A plenty of theories on the origin of genetic codes have been proposed so far, yet all ignored the energetic driving force, its relation to the biochemical system, and most importantly, the missing “matchmaker” between proteins and nucleic acids. Here, a new hypothesis is proposed, according to which ATP is at the origin of the primordial genetic code by driving the coevolution of the genetic code with the pristine biochemical system. This hypothesis aims to show how the genetic code was produced e.g. by photochemical reactions in a protocell that derived from a lipid vesicle enclosing various life’s building blocks (e.g. nucleotides and peptides). At extant cell, ATP is the only energetic product of photosynthesis, and is at the energetic heart of the biochemical systems. ATP could energetically form and elongate chains of both polynucleotides and polypeptides, thus acting a “matchmaker” between these two bio-polymers and eventually mediating precellular biochemical innovation from energy transformation to informatization. ATP was not the only one that could drive the formation of polynucleotides and polypeptides, but favored by precellular selection. The protocell innovated a photosynthetic system to produce ATP efficiently and regularly with the aids of proteins and RNA/DNA. The completion of permanently recording the genetic information by DNA marked the dawn of cellular life operated by Darwinian evolution. The ATP hypothesis assumes or supports the photochemical origin of life, shedding light on the origins of both photosynthetic and biochemical systems, which remain largely unknown thus far. Based on the ATP hypothesis, virus (like the new coronavirus) could not be the earliest life on Earth, as it has neither biochemical systems nor lipid bilayer membrane that provided relatively isolated environment for the development of protobiochemical reactions, although it owns the genetic code of a cellular life. Virus could not be a bridge between life and non-life, but is an anti-life substance, as it depletes cellular material for its own replication, and then spreads by destroying the host cells. It can be imagined that if cellular life are completely wiped out by the virus, the complete destruction of life on Earth would be inevitable.

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The ATP Hypothesis Discovers the Missing “Matchmaker” between Proteins and Nucleic Acids

10.20944/preprints202003.0419.v9 ◽

2020 ◽

Author(s):

Ping Xie

Keyword(s):

Nucleic Acids ◽

Genetic Code ◽

Photochemical Reactions ◽

Host Cells ◽

Darwinian Evolution ◽

Lipid Vesicle ◽

Biochemical System ◽

Cellular Life ◽

Biochemical Systems ◽

Life On Earth

A plenty of theories on the origin of genetic codes have been proposed so far, yet all ignored the energetic driving force, its relation to the biochemical system, and most importantly, the missing “matchmaker” between proteins and nucleic acids. Here, a new hypothesis is proposed, according to which ATP is at the origin of the primordial genetic code by driving the coevolution of the genetic code with the pristine biochemical system. This hypothesis aims to show how the genetic code was produced e.g. by photochemical reactions in a protocell that derived from a lipid vesicle enclosing various life’s building blocks (e.g. nucleotides and peptides). At extant cell, ATP is the only energetic product of photosynthesis, and is at the energetic heart of the biochemical systems. ATP could energetically form and elongate chains of both polynucleotides and polypeptides, thus acting a “matchmaker” between these two bio-polymers and eventually mediating precellular biochemical innovation from energy transformation to informatization. ATP was not the only one that could drive the formation of polynucleotides and polypeptides, but favored by precellular selection. The protocell innovated a photosynthesis system to produce ATP efficiently and regularly with the aids of proteins and RNA/DNA. The completion of permanently recording the genetic information by DNA marked the dawn of cellular life operated by Darwinian evolution. The ATP hypothesis assumes or supports the photochemical origin of life, shedding light on the origins of both photosynthetic and biochemical systems, which remains largely unknown thus far. Based on ATP hypothesis, virus (like the new coronavirus) could not be the earliest life on Earth, as it has neither biochemical systems nor lipid bilayer membrane that provided relatively isolated environment for the development of protobiochemical reactions, although it owns the genetic code of a cellular life. Virus could not be a bridge between life and non-life, but is an anti-life substance, as it depletes cellular material for its own replication, and then spreads by destroying the host cells. It can be imagined that if cellular life are completely wiped out by the virus, the complete destruction of life on Earth would be inevitable.

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Low-Digit and High-Digit Polymers in the Origin of Life

Life ◽

10.3390/life9010017 ◽

2019 ◽

Vol 9 (1) ◽

pp. 17 ◽

Cited By ~ 1

Author(s):

Peter Strazewski

Keyword(s):

Nucleic Acids ◽

Information Transfer ◽

Test Tube ◽

Linear Polymers ◽

Fine Grained ◽

Catalytic Potential ◽

Cellular Life ◽

Evolution Of Life ◽

Compositional Diversity ◽

Life On Earth

Extant life uses two kinds of linear biopolymers that mutually control their own production, as well as the cellular metabolism and the production and homeostatic maintenance of other biopolymers. Nucleic acids are linear polymers composed of a relatively low structural variety of monomeric residues, and thus a low diversity per accessed volume. Proteins are more compact linear polymers that dispose of a huge compositional diversity even at the monomeric level, and thus bear a much higher catalytic potential. The fine-grained diversity of proteins makes an unambiguous information transfer from protein templates too error-prone, so they need to be resynthesized in every generation. But proteins can catalyse both their own reproduction as well as the efficient and faithful replication of nucleic acids, which resolves in a most straightforward way an issue termed “Eigen’s paradox”. Here the importance of the existence of both kinds of linear biopolymers is discussed in the context of the emergence of cellular life, be it for the historic orgin of life on Earth, on some other habitable planet, or in the test tube. An immediate consequence of this analysis is the necessity for translation to appear early during the evolution of life.

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Seismic stratigraphy of Late Quaternary glacial to marine sediments offshore Bornholm, southern Baltic Sea

Sedimentary Geology ◽

10.1016/0037-0738(95)00056-9 ◽

1996 ◽

Vol 102 (1-2) ◽

pp. 3-21 ◽

Cited By ~ 8

Author(s):

L. Perini ◽

T. Missiaen ◽

G.G. Ori ◽

M. de Batist

Keyword(s):

Baltic Sea ◽

Marine Sediments ◽

Late Quaternary ◽

Seismic Stratigraphy ◽

Southern Baltic Sea ◽

Southern Baltic

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Integrative single-cell and cell-free plasma RNA transcriptomics elucidates placental cellular dynamics

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1710470114 ◽

2017 ◽

Vol 114 (37) ◽

pp. E7786-E7795 ◽

Cited By ~ 83

Author(s):

Jason C. H. Tsang ◽

Joaquim S. L. Vong ◽

Lu Ji ◽

Liona C. Y. Poon ◽

Peiyong Jiang ◽

...

Keyword(s):

Nucleic Acids ◽

Single Cell ◽

Human Placenta ◽

Single Cells ◽

Specific Gene ◽

Hypertensive Disorder ◽

Cellular Dynamics ◽

Maternal Cell ◽

Plasma Rna ◽

Free Plasma

The human placenta is a dynamic and heterogeneous organ critical in the establishment of the fetomaternal interface and the maintenance of gestational well-being. It is also the major source of cell-free fetal nucleic acids in the maternal circulation. Placental dysfunction contributes to significant complications, such as preeclampsia, a potentially lethal hypertensive disorder during pregnancy. Previous studies have identified significant changes in the expression profiles of preeclamptic placentas using whole-tissue analysis. Moreover, studies have shown increased levels of targeted RNA transcripts, overall and placental contributions in maternal cell-free nucleic acids during pregnancy progression and gestational complications, but it remains infeasible to noninvasively delineate placental cellular dynamics and dysfunction at the cellular level using maternal cell-free nucleic acid analysis. In this study, we addressed this issue by first dissecting the cellular heterogeneity of the human placenta and defined individual cell-type–specific gene signatures by analyzing more than 24,000 nonmarker selected cells from full-term and early preeclamptic placentas using large-scale microfluidic single-cell transcriptomic technology. Our dataset identified diverse cellular subtypes in the human placenta and enabled reconstruction of the trophoblast differentiation trajectory. Through integrative analysis with maternal plasma cell-free RNA, we resolved the longitudinal cellular dynamics of hematopoietic and placental cells in pregnancy progression. Furthermore, we were able to noninvasively uncover the cellular dysfunction of extravillous trophoblasts in early preeclamptic placentas. Our work showed the potential of integrating transcriptomic information derived from single cells into the interpretation of cell-free plasma RNA, enabling the noninvasive elucidation of cellular dynamics in complex pathological conditions.

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Methane fluxes in marine sediments quantified through core analyses and seismo-acoustic mapping (Bornholm Basin, Baltic Sea)

Geochimica et Cosmochimica Acta ◽

10.1016/j.gca.2018.07.040 ◽

2018 ◽

Vol 239 ◽

pp. 255-274 ◽

Cited By ~ 7

Author(s):

Karen Marie Hilligsøe ◽

Jørn Bo Jensen ◽

Timothy G. Ferdelman ◽

Henrik Fossing ◽

Laura Lapham ◽

...

Keyword(s):

Baltic Sea ◽

Marine Sediments ◽

Bornholm Basin ◽

Methane Fluxes ◽

Acoustic Mapping

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Three Lives and Astrobiology

Social and Conceptual Issues in Astrobiology ◽

10.1093/oso/9780190915650.003.0004 ◽

2020 ◽

pp. 57-78 ◽

Cited By ~ 1

Author(s):

Lucas Mix

Keyword(s):

Anthropic Principle ◽

Biological Organization ◽

Cellular Life ◽

Hard Problems ◽

Life On Earth ◽

Different Origins ◽

Three Lives

This chapter explores the concept of life across traditions, from science to philosophy to theology. The term “life” covers at least three constellations of meaning or life-concepts: biological life, internal life, and rational life. Biological life shares traits with all cellular life on Earth (archaea, eubacteria, and eukarya). Internal or conscious life shares subjective interiority with humans. Rational life shares intellect with all minds that can distinguish truth from non-truth. These three lives possess different origins, extents, and futures. The chapter then identifies three distinct “hard problems of life” relating to the origin and extent of biological organization, consciousness, and reason: moving from non-life to life, from life to sentience, and from sentience to rationality. The Drake equation, the Fermi paradox, and the anthropic principle provide concrete examples in astrobiology.

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