The second half of the chapter quotes a formula about kingship and it is the harshest description of the office in the book. One who takes on the filth of the state is called the lord of the altars of soil and grain. One who takes on the ill fortune of the state is called the king of the world.
The two titles are real. The altars of soil and grain were the central shrines of a state, and the phrase stands for the state itself in ordinary usage of the period, so lord of the altars is a formal designation of a ruler rather than an invention.
What the chapter attaches to those titles is absorption of what nobody wants. The words rendered filth and ill fortune are strong, and the claim is that legitimacy is earned by taking on a state's disgrace and its calamities rather than by receiving its revenue and its honours. Chapter thirty-nine gives the same argument from the other side when it explains why rulers call themselves orphaned and unworthy.
Read with the water passage above it, the chapter is consistent. Water occupies the low place and receives what runs down to it, and the ruler described here is doing the same thing with the moral and material waste of a polity.
The chapter closes with four words that could stand as a note on the whole book: straight words seem to say the opposite. Every reader who has found the text perverse is told, in its second to last chapter, that the perversity is the expected reading and not a misunderstanding.