Microhabitat-specificity of the hindgut microbiota in higher termites
Mikaelyan, Aram
Termites are a group of eusocial insects in the superorder
Dietyaptera, believed to have evolved from a lineage of ancient
cockroach-like ancestors 150 million years ago. They play an important
role in the breakdown of dead plant material, with the help of
microorganisms harboured in the gut. The termites can be classified into
flagellate-harbouring lower termites and flagellate-free higher termites. In
comparison to the lower termites, the higher termites have undergone
immense phylogenetic and dietary diversification, that has led to major
changes in their gut structure. This diversification in the host is reflected in
differences in their gut communities.
To understand how host phylogeny and diet help shape bacterial
communities in higher termites, I conducted an extensive pyrosequencingbased
community survey of the gut communities of the major higher
termite subfamilies, Macrotermitinae, Termitinae, and Nasutitermitinae.
First, I constructed clone libraries and calculated phylogenetic trees for
relevant bacterial taxa found in a variety of higher termites. The node
information in these trees was used to provide a robust phylogenetic
backbone for the accurate taxonomic assignment of the shorter
pyrosequences. The analysis revealed that phylogenetically related
termites in general, have similar community structure. However, one of the
wood-feeding termites showed a greater similarity in gut community
structure to other wood-feeders, in spite of not being phylogenetically
related to them. The results suggest that although host phylogeny appears
to be the major driving force in the determination of gut community
membership, host diet can significantly contribute to community structure.
However, far from being a homogenous environment, the higher
termite gut is a highly structured habitat and shows the presence of
spatially separated and physicochemically distinct compartments.
Conditions unique to each compartment, playa significant role in shaping
distinct compartment-specific communities. I used pyrotag sequencing to
conduct an in-depth analysis of the communities of gut compartments
from termites belonging to the families Termitinae and Nasutitermitinae. I
found that homologous compartments from closely related termites are
more similar in their community structure than adjacent compartments
from the same termite. Based on our results, we hypothesize that similar
ecological conditions such as increased alkalinity in the anterior gut, drive
community structure in the gut compartments, and are reflected in overall
hindgut community structure as well.
The paunch (or P3 compartment) is the most voluminous of all
hindgut compartments in wood-feeding higher termites, and is densely
colonized by bacteria. Studies have shown that cellulase activity in the
hindgut is particle-associated and possibly of bacterial origin. By
fractionation of particles in the paunch lumen, using density-dependent
centrifugation , I was able to show that the fraction enriched in wood fibers
contributes substantially to the total cellulase activity in the hindgut. Using
pyrosequencing, I examined the bacterial communities associated with the
wood fibers in two wood-feeding members of the Nasutitermitinae. The
results revealed the presence of a distinct cellulolytic fiber-associated
community, primarily composed of the phyla TG3, Fibrobacteres and
Spirochaetes. This fiber-associated community appears to have filled the
niche for cellulose digestion, vacated by the flagellates.
Lastly, the gut wall in termites is one of the major habitats in the gut,
and home to an endospore-forming filamentous bacterium called
'Candidatus Arthromitus'. Due to the lack of a cultured isolate, the phylogenetic identity of 'Arthromitus' was disputed, and often confused
with similar filamentous bacteria from mammalian guts. Phylogenetic
analysis of picked filaments reveals 'Candidatus Arthromitus' to be a
diverse clade of bacteria, found widely among arthropods, that is distinct
from the segmented filamentous sequences recovered from mammalian
guts.
Philipps-Universität Marburg
Life sciences
opus:5309
https://doi.org/10.17192/z2013.0753
urn:nbn:de:hebis:04-z2013-07532
opus:5309
Biologie
2014-06-25
monograph
ppn:341684791
Die Termiten sind eine Gruppe eusozialer Insekten in der
Superordnung Dictyoptera und haben sich vermutlich vor 150 Millionen
Jahren aus einer Linie Schaben-ahnlicher Vorfahren entwickelt. Sie
spielen beim Abbau toter Pflanzen masse eine wichtige Rolle, wobei sie
von in ihrem Darm lebenden Bakterien unterstotzt werden. Man
unterscheidet zwischen den Flagellaten beherbergenden niederen
Termiten und den Flagellaten-freien hOheren Termiten. 1m Gegensatz zu
den niederen Termiten vollzogen die hbheren Termiten eine immense
phylogenetische und diatische Diversifizierung, die grundlegende
Veranderungen ihrer Darmstruktur zur Feige hatte. Diese Diversifizierung
im Wirt tritt in Unterschieden der Darmmikrobiota zu Tage.
Urn zu verstehen , wie Phylogenie und Erna.hrungsweise des Wirtes
die bakteriellen Gemeinschaften in h6heren Termiten formen , fUhrte ich
eine extensive Pyrosequenzierung-basierte Vergleichsstudie der
Darmgemeinschaften in den wichtigsten Unterfamilien der Termiten,
Macrotermitinae, Termitinae und Nasutitermitinae, durch. Zunachst
konstruierte ich Klonbibliotheken und berechnete phylogenetische Saume
fUr relevante bakterielie Taxa aus verschiedenen h6heren Termiten . Die
Knotenpunkt-Informationen aus diesen Baumen dienten als robustes
phlylogenetisches ROckgrat fOr die korrekte taxonomische Zuordnung der
kOrzeren Pyrosequenzen. Die Analyse ergab, dass phylogenetisch
verwandte Termiten im Aligemeinen eine ahnliche Gemeinschaftsstruktur
aulweisen. Eine der holzfressenden Termiten zeigte jedoch eine gr6~ere
Ahnlichkeit zu anderen holzfressenden Arten, ohne mit ihnen
phylogenetisch verwandt zu sein. Die Ergebnisse leg en nahe, dass die
Phylogenie des Wirtes zwar die wesentliche treibende Kraft bei der Festlegung der Darmgemeinschaft darstellt, die Ernahrungsweise des
Wirtes jedoch signifikant zur Gemeinschaftsstruktur beitragen kann.
Der Darm der h6heren Termiten, mitnichten eine homogene
Umgebung, bildet ein hoch strukturiertes Habitat und weist Ortlich
getrennte und physiochemisch verschiedene Kompartimente auf. In jedem
Kompartiment bestimmen einzigartige Bedingungen die spezifische
Gemeinschaft. Mittels Pyrotag-Sequenzierung fOhrte ich eine ausfOhrliche
Analyse der Kompartiment-spezifischen Gemeinschaften in Termiten der
Familien Termitinae und Nasutitermitinae durch. Ich fand heraus, dass
homo loge Kompartimente nah verwandter Termiten einander ahnlicher
waren als benachbarte Kompartimente derselben Termite. Basierend auf
unseren Ergebnissen vermuten wir, dass ahnliche dkologische
Bedingungen, wie beispielsweise erMhte Alkalinitat im Vorderdarm, die
Gemeinschaftsstruktur in den Darmkompartimenten beeinflussen und
ebenfalls in der Gemeinschaftsstruktur des Dickdarms insgesamt
reflektiert werden.
Der Pansen (oder P3-Kompartiment) ist volumenmal]ig der gr61]te
Dickdarmabschnitt in holzfressenden h6heren Termiten und ist vollstandig
mit Holzfasern und Bakterien gefOllt. Ober den Beitrag von Bakterien zum
Celluloseverdau ist jedoch wenig bekannt. Durch Fraktionierung der
Partikel im Lumen des Pansen mittels Dichtegradientenzentrifugation
konnte ich zeigen, dass die in Holzfasern angereicherte Fraktion
substantiell zur gesamten Cellulase-Aktivitat beitrug. Mittels
Pyrosequenzierung untersuchte ich die mit den Holzfasern assQziierten
bakteriellen Gemeinschaften in zwei holzfressenden Vertretern der
Nasutitermitinae. Die Ergebnisse offenbarten die Anwesenheit einer
eindeutig cellulolytischen, Faser-assoziierten Gemeinschaft, die vor allem
aus den Phyla TG3, Fibrobacteres und Spirochaetes bestand. Diese
Faser-assoziierte Gemeinschaft scheint die von den Flagellaten
verlassene Nische des Celluloseverdaus zu besetzen.
Die Darmwand der Termiten ist eines der wichtigsten Habitate des Darms
und beherbergt ein Endosporen-bildendes filament6ses Bakterium
namens "Candidalus Arthromitus", Mangels eines kultivierten Isolates
wurde die phylogenetische Identitat von 'Arthromitus' angezweifelt und oft
mit ahnlichen filament6sen Bakterien aus Saugetierdarmen verwechselt.
Phylogenetische Analyse einzeln ausgewahlter Filamente zeigte
Candidatus Arthromitus als einen diversen Stamm von Bakterien, der
unter Arthropoden weit verbreitet ist und sich deutlich von segmentierten
filamentDsen Sequenzen aus Saugetierdarmen unterscheidet.
ths
Prof. Dr.
Brune
Andreas
Brune, Andreas (Prof. Dr.)
Publikationsserver der Universitätsbibliothek Marburg
Universitätsbibliothek Marburg
Mikaelyan, Aram
Mikaelyan
Aram
Termiten
Fachbereich Biologie
https://doi.org/10.17192/z2013.0753
2014-06-25
doctoralThesis
Life sciences
Biowissenschaften, Biologie
Microhabitat
Termitendarm
urn:nbn:de:hebis:04-z2013-07532
Microhabitat-specificity of the hindgut microbiota in higher termites
Termites are a group of eusocial insects in the superorder
Dietyaptera, believed to have evolved from a lineage of ancient
cockroach-like ancestors 150 million years ago. They play an important
role in the breakdown of dead plant material, with the help of
microorganisms harboured in the gut. The termites can be classified into
flagellate-harbouring lower termites and flagellate-free higher termites. In
comparison to the lower termites, the higher termites have undergone
immense phylogenetic and dietary diversification, that has led to major
changes in their gut structure. This diversification in the host is reflected in
differences in their gut communities.
To understand how host phylogeny and diet help shape bacterial
communities in higher termites, I conducted an extensive pyrosequencingbased
community survey of the gut communities of the major higher
termite subfamilies, Macrotermitinae, Termitinae, and Nasutitermitinae.
First, I constructed clone libraries and calculated phylogenetic trees for
relevant bacterial taxa found in a variety of higher termites. The node
information in these trees was used to provide a robust phylogenetic
backbone for the accurate taxonomic assignment of the shorter
pyrosequences. The analysis revealed that phylogenetically related
termites in general, have similar community structure. However, one of the
wood-feeding termites showed a greater similarity in gut community
structure to other wood-feeders, in spite of not being phylogenetically
related to them. The results suggest that although host phylogeny appears
to be the major driving force in the determination of gut community
membership, host diet can significantly contribute to community structure.
However, far from being a homogenous environment, the higher
termite gut is a highly structured habitat and shows the presence of
spatially separated and physicochemically distinct compartments.
Conditions unique to each compartment, playa significant role in shaping
distinct compartment-specific communities. I used pyrotag sequencing to
conduct an in-depth analysis of the communities of gut compartments
from termites belonging to the families Termitinae and Nasutitermitinae. I
found that homologous compartments from closely related termites are
more similar in their community structure than adjacent compartments
from the same termite. Based on our results, we hypothesize that similar
ecological conditions such as increased alkalinity in the anterior gut, drive
community structure in the gut compartments, and are reflected in overall
hindgut community structure as well.
The paunch (or P3 compartment) is the most voluminous of all
hindgut compartments in wood-feeding higher termites, and is densely
colonized by bacteria. Studies have shown that cellulase activity in the
hindgut is particle-associated and possibly of bacterial origin. By
fractionation of particles in the paunch lumen, using density-dependent
centrifugation , I was able to show that the fraction enriched in wood fibers
contributes substantially to the total cellulase activity in the hindgut. Using
pyrosequencing, I examined the bacterial communities associated with the
wood fibers in two wood-feeding members of the Nasutitermitinae. The
results revealed the presence of a distinct cellulolytic fiber-associated
community, primarily composed of the phyla TG3, Fibrobacteres and
Spirochaetes. This fiber-associated community appears to have filled the
niche for cellulose digestion, vacated by the flagellates.
Lastly, the gut wall in termites is one of the major habitats in the gut,
and home to an endospore-forming filamentous bacterium called
'Candidatus Arthromitus'. Due to the lack of a cultured isolate, the phylogenetic identity of 'Arthromitus' was disputed, and often confused
with similar filamentous bacteria from mammalian guts. Phylogenetic
analysis of picked filaments reveals 'Candidatus Arthromitus' to be a
diverse clade of bacteria, found widely among arthropods, that is distinct
from the segmented filamentous sequences recovered from mammalian
guts.
2013
Philipps-Universität Marburg
https://archiv.ub.uni-marburg.de/diss/z2013/0753/cover.png
English
Spezifikation des Mikrohabitats der Enddarmmikroben in höheren Termiten
application/pdf
2013-11-19
Mikrohabitat
Termite Gut
Termites
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