PhD Thesis - Summary

PhD Thesis - Summary

The microbial Party – Electro, Hard Rock, and Heavy Metal

How geomicrobiology helps us to understand climate changes.

* This article is more detailled in German*

Climate change, greenhouse gases and their effects

Understanding climate changes – this is one of the great challenges for humankind in the 21^st century. Greenhouse gases (GHGs) such as nitrous oxide (N₂O) are one of the main drivers of climate changes. Besides agricultural farmlands, coastal sediments were identified as an additional significant N₂O sources. In iron-containing coastal sediments bacteria can form N₂O during the degradation of nitrate. So-called iron-cycling bacteria (FeB) occur in complex communities and can metabolize iron minerals ("heavy metal" & "hard rock"). Until now, the contribution of the abiotic processes - besides microbial mediated processes - to the global N₂O budget was unknown. My research study is the first worldwide that has quantified the geochemical formation of N₂O by iron in coastal sediments. These findings will help to improve our understanding of climate changes and its consequences.

Coastal sediments as important N2O source

Some key factors of climate changes are already known (solar cycles, precision of the Earth's axes, etc.). In addition, the formation of GHGs is one of the most important origins of climate changes. For example, GHGs such as carbon dioxide (CO₂), methane, ozone, and N₂O can cause great damage in the stratosphere. In 1998, coastal marine habitats were identified as important N₂O sources. Sandy sediments are representative of about 70% of all global shelf sediments and are expected to release up to 1.9 teragrams of N₂O-N per year. In the future, the release of N₂O could even increase further due to the extensive use of nitrate fertilizers. Rainfall can wash out the nitrate from the farmland, which then deposits in the nearby sediments. The activity of nitrate-degrading bacteria living in these sediments and abiotic reactions can form N₂O. This leads to the central research question: To what extent do microbial and abiotic processes contribute to the formation of N₂O in coastal sediments?

Biogeochemistry of iron-containing sediments

Redoxzonen — Abbildung 1: Der geschichtete Aufbau von typischen Küstensedimenten mit der oxischen Zone (blau: mit Sauerstoff) und der anoxischen Zone (rot: ohne Sauerstoff). In den oberen Schichten der Sedimente findet u.a. Photosynthese statt, weiter unten wird u.a. Nitrat abgebaut, sowie Eisen(II) und Eisen(III) umgesetzt. Der Sedimentkern zeigt marines Küstensediment. (c) Dr. Julia M. Otte

The biogeochemistry of coastal sediments is usually characterized by vertical gradients of electron donors and electron acceptors. During microbial conversion processes, the electron acceptors are consumed in a typical order. The degradation of organic compounds with O₂ provides the highest amount of energy and therefore O₂ is typically consumed first, followed by nitrate, iron(III) and finally CO₂. Iron is after O₂, silicon, and aluminium one of the most common elements on earth and is involved in a variety of metabolic and chemical processes. In order to generate energy for cellular processes and growth, FeB convert iron between iron(II) and iron(III). FeB are widespread in nature and contribute to all major biogeochemical cycles.

Fe Zyklus — Abbildung 2: Der Eisenkreislauf in Salz- und Süßwasser-Sedimenten besteht aus zwei Prozessen: Eisen(II) zu Eisen(III) und Eisen(III) zu Eisen(II). Der Eisenkreislauf wird durch biotische (von Bakterien gesteuerte; linker Kreislauf) und abiotische (geochemische; rechter Kreislauf) Reaktionen vorangetrieben. Es gibt vier verschiedene Gruppen von Eisenbakterien: 1) Sauerstoff-liebende, 2) Licht-abhängige, 3) Nitrat-abbauende und 4) Eisen(III)-liebende Eisenbakterien. (c) Dr. Julia M. Otte

*See German webpage*

Unexpected distribution of iron-cycling microorganisms in coastal sediments

Veretilung von FeOx — Figure 1: Schematic representation of the expected and measured microbial distributions in representative coastal sediments. About 75% of the total bacterial community is orientated by geochemical layers. Active iron-cycling bacteria do not follow the expected distribution. (c) Dr. Julia M. Otte

Until now, the natural distribution of active FeB in coastal sediments was unknown. As a graduate student in Andreas Kappler's and Sara Kleindienst's laboratory at the University of Tübingen, I investigated the diversity, distribution, and activity of FeB in representative sediments: freshwater sediments from Lake Constance (Germany) and marine sediments from Aarhus Bay (Denmark). The microbial community was characterized at the O₂-rich and O₂-poor interface of the upper 3 cm. Geochemical profiles of iron, O₂, nitrate, and light showed a specific stratification of the investigated sediments. This stratification could explain 75-85% of the vertical distribution of all sediment bacteria (Figure 1). Therefore, such a distribution was also expected for FeB. Instead, a homogenous distribution of the active FeB was found in the investigated sediment depths, which means that the active FeB do not orient themselves by geochemical gradients. This behavior can be explained by the fact that the FeB i) are mobile and can "sleep" until better conditions are achieved, ii) live in microniches filled with O₂ or nitrate, iii) can metabolize different substances, or iv) interact with the recently discovered cable bacteria (CB).

Survival strategy — Abbildung 4: Mögliche Erklärungen für die homogene Verteilung von aktiven Eisenbakterien. i) Physikalische Durchmischung durch Wellen oder Würmern, ii) Eisenbakterien können „schlafen“, iii) Eisenbakterien sind mobil, iv) Eisenbakterien finden kleine Nischen, die mit Sauerstoff oder Nitrat gefüllt sind, v) Eisenbakterien sind nicht wählerisch, sondern können verschiedene „Nahrungsmittel“ aufnehmen, vi) Eisenbakterien interagieren mit Kabelbakterien und nutzen diese als „Elektronen-Tankstelle“ oder „Elektronen-Mülleimer“. e- = Elektronen, O2 = Sauerstoff. (c) Dr. Julia M. Otte

*See German webpage*

One potential explanation - the extraordinary microbial "Electro Party"

Abbildung 5: Die „Kabelbakterien-Tankstelle“ in marinen Küstensedimenten. (c) Dr. Julia M. Otte

CB are able to transport electrons over long distances in sediments and indeed function like electric cables! With my sequencing data I could show for the first time that CB and FeB are both active in the same sediment layers. This means in detail: the iron(II)-oxidizing bacteria may be able to transfer electrons to the CB and the iron(III)-reducing bacteria can take up electrons with the help of the CB. Thus, the extraordinary "electrogenic connection" of CB and FeB could explain the special distribution pattern of "rocky" FeB in the investigated “hard rock” and “heavy metal”-containing sediments.

Chemical and Biotic — Abbildung 6: Der Einfluss von geochemischen (Chemodenitrifikation) und bakteriellen Prozessen (Denitrifikation) auf die Treibhausgasentwicklung (hier: N2O). Um in einer komplexen Umweltprobe wie Küstensediment die geochemischen und bakteriellen Prozesse zu trennen, kann die Umweltprobe mithilfe von verschiedenen Verfahren sterilisiert werden. Damit kann der unbekannte Beitrag der geochemischen Prozesse zum globalen N2O Budget bestimmt werden. (c) Dr. Julia M. Otte

*See German webpage*

Geochemical activities in coastal sediments - the unknown contribution to the global N2O budget

N cycle — Abbildung 7: Beiträge zum globalen N2O Budget. Bisher gab es zahlreiche Studien zu biotischen N2O bildenden Reaktionen, die von Bakterien umgesetzt worden sind (in der Abbildung sind verschieden farbige Bakterien dargestellt). Der Beitrag an geochemischen (abiotischen) Prozessen zum globalen N2O Budget war bisher unbekannt. In meiner Doktorarbeit konnte nachgewiesen werden, dass die Chemodenitrifikation ca. 20% des globalen N2O Budget in Küstensedimenten bildet. (c) Dr. Julia M. Otte

CB and nitrate-degrading FeB - which are active in all investigated sediment layers - can use nitrate in the absence of O₂ and thus contribute to the degradation of nitrate followed by nitrite and N₂O formation. The homogeneous distribution patterns of CB and FeB also have a major influence on the surrounding geochemistry. Geochemical processes are also involved in the iron and nitrogen cycle. For example, the rapid abiotic reduction of nitrite by iron(II) can lead to an abiotic production of N₂O (chemodenitrification). Until now, the specific contribution of chemodenitrification to the global N₂O budget was unknown. With my experiments I was able to determine the N₂O formation in natural (microbially + geochemically active) and sterile (only geochemically active) sediment. The comparison of natural and sterile sediment showed that a remarkable amount of at least 15-25% of the total N₂O formation was caused by chemodenitrification, while 75-85% of the total N₂O concentration was formed by microbial processes. This suggests that the process of chemodenitrification can contribute significantly to global N₂O formation and also affect the microbial community.

Summary

These new findings improve our understanding of bacterial and geochemical processes leading to N₂O formation. Especially, in highly complex nonlinear contexts such as climate changes, it is important to identify all the relevant parameters and take them into account when we are developing climate models. We have a huge responsibility to future generations.